Magnetoreception in Birds and Its Use for Long-Distance Migration

Abstract

The Earth's magnetic field provides potentially useful information, which birds could use for directional and/or positional information. It has been clearly demonstrated that birds are able to sense the compass direction of the Earth's magnetic field and that they can use this information as part of a compass sense. Magnetic information could also be useful as part of a map sense, and there is a growing body of evidence that birds are able to determine their approximate position on the Earth on the basis of geo-magnetic cues. In addition to direct uses for orientation and navigation, magnetic information also seems to be able to influence other physiological processes, such as fattening and migratory motivation, as a trigger for changes in behavior. Although the behavioral responses to geomagnetic cues are relatively well understood, the physiological mechanisms enabling birds to sense the Earth's magnetic field are only starting to be understood, and understanding the magnetic sense(s) of animals, including birds, remains one of the most significant unsolved problems in biology. It is very challenging to sense magnetic fields as weak as that of the Earth using only biologically available materials. Only two basic mechanisms are considered theoretically viable in terrestrial animals: iron-mineral-based magnetoreception and radical-pair based magnetoreception. On the basis of current scientific evidence, iron-mineral-based magnetorecep-tion and radical-pair-based magnetoreception mechanisms seem to exist in birds, but they seem to be used for different purposes. Plausible primary sensory molecules and a few brain areas involved in processing magnetic information have been identified in birds for each of these two types of magnetic senses. Nevertheless, we are still far away from understanding the detailed function of any of the at least two different magnetic senses existing in some if not all bird species, and, at present, no primary sensory structure has been identified beyond reasonable doubt to be the source of avian magnetoreception. This is an exciting but challenging field in which several major discoveries are likely to be made in the next 1–2 decades.

Full text

113
Sturkie’s Avian Physiology.
Copyright © 2015 Elsevier Inc. All rights reserved.
Magnetoreception in Birds and Its Use for
Long-Distance Migration*
Henrik Mouritsen
Institut für Biologie und Umweltwissenschaften, Universität Oldenburg, Oldenburg, Germany; Research Centre for Neurosensory Sciences,
University of Oldenburg, Oldenburg, Germany
* Because our knowledge of magnetoreception did not change dramatically over the last few months, there is significant text and content overlap between
the present chapter and a chapter focusing on magnetoreception in all kinds of organisms and titled “The Magnetic Senses,” which I recently wrote for the
textbook Neurosciences: Mouritsen, H., 2013. The magnetic senses. In: Galizia, C.G., Lledo, P.M. (Eds), Neurosciences—From Molecule to Behavior: A
University Textbook. © Springer-Verlag Berlin Heidelberg, pp. 427–443, doi: 10.1007/978-3-642-10,769-6_20. Springer Verlag has permitted the reuse of
significant parts of the Neurosciences textbook chapter text and figures in the present chapter. Specific references to this text are not given at every location
where text is reused because such references would compromise readability and could be misunderstood to be referring to primary research findings.
Chapter 8
8.1 INTRODUCTION
The Earth’s magnetic field provides potentially useful
information, which birds could use for directional and/
or positional information. It has been clearly demon-
strated that birds are able to sense the compass direction of
the Earth’s magnetic field and that they can use this infor-
mation as part of a compass sense. Magnetic information
could also be useful as part of a map sense, and there is a
growing body of evidence that birds are able to determine
their approximate position on the Earth on the basis of geo-
magnetic cues. In addition to direct uses for orientation and
navigation, magnetic information also seems to be able to
influence other physiological processes, such as fattening
and migratory motivation, as a trigger for changes in behav-
ior. Although the behavioral responses to geomagnetic cues
are relatively well understood, the physiological mecha-
nisms enabling birds to sense the Earth’s magnetic field are
only starting to be understood, and understanding the mag-
netic sense(s) of animals, including birds, remains one of
the most significant unsolved problems in biology. It is very
challenging to sense magnetic fields as weak as that of the
Earth using only biologically available materials. Only two
basic mechanisms are considered theoretically viable in ter-
restrial animals: iron-mineral-based magnetoreception and
radical-pair based magnetoreception. On the basis of cur-
rent scientific evidence, iron-mineral-based magnetorecep-
tion and radical-pair-based magnetoreception mechanisms
seem to exist in birds, but they seem to be used for different
purposes. Plausible primary sensory molecules and a few
brain areas involved in processing magnetic information
have been identified in birds for each of these two types of
magnetic senses. Nevertheless, we are still far away from
understanding the detailed function of any of the at least
two different magnetic senses existing in some if not all bird
species, and, at present, no primary sensory structure has
been identified beyond reasonable doubt to be the source of
avian magnetoreception. This is an exciting but challeng-
ing field in which several major discoveries are likely to be
made in the next 1–2 decades.
8.2 MAGNETIC FIELDS
Moving electric charges such as electrons produce mag-
netic fields. On the microscopic scale, electron (and
nuclear) spins can generate magnetic fields. On the mac-
roscopic scale, a magnetic field, B, is, for instance, gen-
erated around a wire when current runs through it. The
magnetic field at a given location can be described as a
three-dimensional (3D) vector for which the strength, B, is
measured as magnetic flux density using the unit “Tesla”
(T), 1 T = 1 (V*s)/m2 = 1 (N*s)/(C*m) = 10,000 Gauss
(V = Volt, s = second, m = meter, N = Newton, C = Cou-
lomb). Some materials, which are called “ferromagnetic,”
can be permanently magnetized by a magnetic field, and
this magnetization remains after the magnetizing field has
been removed. Magnetite (Fe3O4), an iron oxide, is a well-
known example of a ferromagnetic mineral (Mouritsen,
2013).

PART | II Sensory Biology and Nervous System Theme
114
8.3 THE EARTH’S MAGNETIC FIELD
The Earth generates its own magnetic field (the geomag-
netic field), which is mostly caused by electric currents in
the liquid outer core of the Earth (the “dynamo effect”).
The magnetic field measured at the Earth’s surface is
similar to the magnetic field one would expect to see if a
large dipole magnet was placed in the center of the Earth
(see Figure 8.1). The Earth’s magnetic field currently has
a magnetic field South Pole near the Earth’s geographic
North Pole (referred to as “Magnetic North” or “Mag-
netic North Pole” in biology). Throughout this chapter,
I will follow the convention used in the bird orientation
research literature and use the term “Magnetic North” or
“Magnetic North Pole” to refer, not to the physical mag-
netic North Pole, but to the magnetic pole located closest
to the geographic North Pole. Likewise, the magnetic field
North Pole near the Earth’s geographic South Pole will be
referred to as “Magnetic South” or “Magnetic South Pole”
(Mouritsen, 2013).
The magnetic field lines leave the Magnetic South Pole
and re-enter the Magnetic North Pole. The polarity of the
magnetic field lines always points toward Magnetic North;
therefore, they can provide a highly reliable directional
reference that can be used as the basis for a magnetic
compass anywhere on planet Earth except at the magnetic
poles. At the magnetic poles, the field lines point directly
into the sky (at the Magnetic South Pole) or directly into
the Earth (at the Magnetic North Pole). At the magnetic
equator, the magnetic field lines are parallel to the Earth’s
surface. The angle between the magnetic field lines and
the Earth’s surface is called “magnetic inclination.” Thus,
magnetic inclination changes gradually from −90° at the
Magnetic South Pole to 0° at the magnetic equator to +90°
at the Magnetic North Pole (see Figure 8.1). The Earth’s
magnetic field intensity ranges from c. 30,000 nT (nano-
Tesla = 10−9 T; 1 T = 1 Vs m−2; 1 nT = 10−5 Gauss) near the
magnetic equator to c. 60,000 nT at the magnetic poles.
Earth-strength magnetic fields are usually measured with
a calibrated three-axial flux-gate magnetometer. In theory,
magnetic inclination and magnetic intensity can be use-
ful for determining one’s position, but, on most parts of
the Earth, magnetic inclination and intensity changes pre-
dominantly from North to South but not much from East to
FIGURE 8.1 The Earth’s magnetic field (the geomagnetic field). Notice that the southern and northern magnetic poles and the magnetic equator do
not coincide with the geographical poles and the geographic equator. Also notice that the magnetic field lines intersect the Earth’s surface at different
angles depending on the magnetic latitude (blue-green lines and vectors). The intersection angle is called the magnetic inclination. Magnetic inclina-
tion is +90° at the Magnetic North Pole (red vector), c. +67° at the latitude of Germany (yellow vector), 0° at the magnetic equator (dark blue vectors),
c. −64° at the latitude of South Africa (orange vector), and −90° at the Magnetic South Pole (magenta vector) (Adapted with permission after Wiltschko
and Wiltschko (1996) and Mouritsen (2013).) The magnetic intensity varies from c. 60,000 nT near the magnetic poles to c. 30,000 nT along the magnetic
equator.

115Chapter | 8 Magnetoreception in Birds and Its Use for Long-Distance Migration
West; therefore, it seems easier to determine latitude than
longitude from geomagnetic field information (Mouritsen,
2013).
The Magnetic North Pole is currently located in northern
Canada, and the Magnetic South Pole is currently located
south of Australia. Consequently, the geographic and mag-
netic poles do not coincide (see Figure 8.1). The devia-
tion between geographic and Magnetic North is called the
“magnetic declination.” Magnetic declination is the angle
between Magnetic North (i.e., the direction in which the
north end of a compass needle points in) and Geographic
North. The declination is positive when Magnetic North
is east of Geographic North and negative when Magnetic
North is west of Geographic North. Declination is mostly
small, but near the magnetic poles declination can pose
a serious problem for navigating birds using a magnetic
compass unless they find a way to compensate for it. On
the other hand, magnetic declination could, in theory, be
a useful parameter to determine, for example, East-West
position if it would be combined with other map cues
(Mouritsen, 2013).
8.4 CHANGING MAGNETIC FIELDS FOR
EXPERIMENTAL PURPOSES
The direction of the magnetic field around a wire can be
determined by the “right hand rule”: If you grasp around
the wire with your right hand so that your thumb is point-
ing in the direction of the current, then the magnetic
field around the wire runs in the direction in which your
fingers are pointing. The magnetic field decreases with
distance as you move away from the wire. If you create
a coil of wire, then the magnetic field created is much
stronger inside of the coil than on the outside of the coil
because many parallel magnetic field lines created by dif-
ferent parts of the wire coincide and thus add up in the
center of the coil. This is the reason why coil construc-
tions are typically used to produce and alter magnetic
fields (Mouritsen, 2013).
The typical coil constructions, which are used to pro-
duce Earth-strength magnetic fields for scientific experi-
ments, are so-called “Helmholtz coils”—a pair of parallel
coils placed one radius apart from each other (Kirschvink,
1991). In a pair of Helmholtz coils, the magnetic field is
very homogeneous within a central space of c. 60% of
the radius of the coils (Kirschvink, 1991). The magnetic
field generated in the center of a pair of Helmholtz coils
is B = (0.9*10−6 T m/A*n*I)/R, where T is the unit Tesla, n
is the number of turns in each coil, I is the current flow-
ing through the coils measured in ampere (A), and R is the
radius of the coils measured in meters (m) (Kirschvink,
1991). One pair of Helmholtz coils can only alter the mag-
netic field along one axis. To make any desired 3D magnetic
field, three pairs of Helmholtz coils oriented perpendicular
to each other are ideally needed. If one adds an artificially
created field to an existing field (such as that of the Earth),
then the resultant field is calculated by simple vector addi-
tion of the two fields (see Figure 8.2; Kirschvink, 1991).
Therefore, it is also possible to use a single pair of Helmholtz
coils to make any 3D magnetic field, but in that case, this
single pair of coils must be oriented very precisely in 3D
space (see Figure 8.2; Mouritsen, 2013).
Although the Helmholtz arrangement is easy to calcu-
late and construct, the central homogeneous space can be
increased to c. 110% of the radius of the coils by using
more elaborate coil designs such as the Merritt-4-coil sys-
tem (Kirschvink, 1991; Zapka et al., 2009, Figure 20.2 in
Mouritsen, 2013). To control for artefacts, one would—
independent of the coil design chosen—expect the coils to
be “double wrapped” (Kirschvink, 1991; Kirschvink et al.,
2010). This means that during construction of the coils,
each coil contains two separate but identically wrapped
wires, each with separate connectors, so that one can either
run current through both halves of the windings in the same
direction (then the magnetic field in the center of the coil
will change), or one can run the current through one half
of the coils in one direction but in the opposite direction
through the second half of the windings. In that case, the
current running through one half of the windings will cre-
ate a magnetic field, which exactly cancels the magnetic
field produced by the other half of the windings, and the
background field is not changed. By using double-wrapped
coils, exactly the same amount of current is sent through the
coils whether the magnetic field is being changed or not.
Double-wrapped coils also allow for truly double-blinded
experiments (Kirschvink, 1991; Zapka et al., 2009; Harris
et al., 2009; Hein et al., 2010, 2011; Engels et al., 2012).
An excellent presentation of the theoretical background
and practical instructions on how to construct various coil
designs for changing Earth-strength magnetic fields can be
found in Kirschvink (1991).
8.5 BIRDS USE INFORMATION FROM
THE EARTH’S MAGNETIC FIELD FOR
ORIENTATION AND NAVIGATION
Orientation and navigation skills are essential for the sur-
vival of all migratory birds. All first-time migrants are faced
with the challenge of finding an unfamiliar wintering area,
often thousands of kilometers away (Berthold, 1991; Mou-
ritsen and Mouritsen, 2000; Mouritsen, 2003). Many bigger
birds are day migratory and travel in groups, which means
that young birds of these species might simply follow expe-
rienced birds that know the way. However, most small song-
birds are night-migratory and travel alone without contact
with their parents. Consequently, all of their navigational
skills must be based on inherited sensory capabilities and
strategies (Mouritsen, 2003). No cues requiring previous

PART | II Sensory Biology and Nervous System Theme
116
experience with the goal can be involved in the orientation
strategies of solitary, first-year migrants. These consider-
ations strongly limit the number of possible orientation cues
to a few classes of globally or at least regionally consistent
cues (Mouritsen, 2003):
1. Celestial cues, including the Sun, the stars, and maybe
the polarized light pattern of the sky
2. Geomagnetic cues
In addition to these cues, some authors have suggested that
chemical cues, including odors, (Wallraff and Andreae,
2000; Wallraff, 2005; Gagliardo et al., 2006, 2008, 2009)
infrasound (sound with frequency below c. 20 Hz; Hag-
strum, 2013 but see Wallraff, 1972; Holland, in press), and/
or Coriolis forces (the phenomenon that moving liquids and
moving air are deflected slightly to the right on the Northern
Hemisphere and slightly to the left on the Southern Hemi-
sphere because of the Earth’s rotation; Coriolis, 1835) might
also be used for orientation and navigation.
However, there seems to be no physiological structure
inside of birds that would enable them to detect the Coriolis
effect with a reasonable signal-to-noise ratio (Rosenblum
et al., 1985; Adair, 1991; Kirschvink et al., 2010). Likewise,
it is difficult to imagine how an inexperienced migrant could
know, in advance, what the infrasound or odor “landscapes”
along its migratory path looks like, and it is difficult to
imagine that the infrasound and/or odor landscapes would
be simple and consistent enough to be used by inexperi-
enced birds as a primary map cue over thousands of kilo-
meters (but see Wallraff and Andreae, 2000). Furthermore,
because the width of the bird’s head is much smaller than
the wavelength of infrasound, it would be challenging for a
N-S axis
E-
W axis
FIGURE 8.2 Magnetic fields are vector fields and can easily be turned with pairs of coils. If we consider the geomagnetic field, it will point toward
North (0°) and have a vertical and a horizontal component. Let’s say that we want to create a magnetic field with the same strength and inclination as the
geomagnetic field but that is turned horizontally 120° counterclockwise. In that case, the vertical component of the field should remain unchanged, and
we only have to consider the two dimensions in the horizontal plane. Let’s say that the Earth’s magnetic field at the relevant location has a horizontal
field component of 18,000 nT pointing toward Magnetic North (black vector). If we want to turn the field to point toward 240° (a 120° counterclockwise
turn, red vector), then we need to produce a magnetic field vector (the blue vector) that connects the tip of the black vector to the tip of the red vector. The
needed field can be produced by a single pair of Helmholtz coils (symbolized by the violet lines) if the coil frames are oriented on the axis defined by
half of the wanted angular turn (in this case 120°/−60°) given that the final wanted intensity should remain unchanged. Simple trigonometry can be used
to calculate the needed field strength, Bblue, of the blue vector. In this case, Bblue = (((cos(αblack)*Bblack) − (cos(αred)*Bred))2 + ((sin(αblack)*Bblack) − (sin(αred-
)*Bred))2)1/2, where αblack = 360°, αred = 240°, and Bblack = Bred = 18,000 nT => Bblue = ((cos(360°)*18,000 nT − cos(240°)*18,000 nT)2 + (sin(360°)*18,000 n
T − sin(240°)*18,000 nT)2)1/2 = (((27,000 nT)2 + (−15,588 nT)2)1/2) = 31,177 nT. If the strength of the final vector should have a different intensity than the
original vector, or if the vertical component also needs to be changed, then again a single pair of coils can, in principle, do the job (the needed calculations
are 3D), but accurately orienting this pair of coils is very difficult in real life. Therefore, if excellent control of static magnetic fields is required, usually
3D systems of perpendicularly oriented coils are used. Because magnetic fields are vector fields, which all need to be added up to get the total resultant
field, instead of producing the direct vector (the blue vector) that connects the tip of the black vector to the tip of the red vector, we can produce two vec-
tors (the dashed blue vectors) along the two coil axes, which in total connect the tip of the black vector to the tip of the red vector. With such systems, each
of the needed vectors is much easier to calculate. The needed N–S component is cos(αblack)*Bblack − cos(αred)*Bred, and the needed E–W component is
sin(αblack)*Bblack − sin(α)*Bred. If one uses a 3D magnetometer oriented with the x-axis toward North and the y-axis toward East, and one just wants to calculate
the values that should be on the display when the wanted field is present, X should read cos(αred)*Bred and Y should read sin(α)*Bred. Thus, in the case of a 120°
counterclockwise turn of the above-mentioned field, X should read cos(240°)*18,000 nT = −9000 nT and Y should read sin(240°)*18,000 nT = −15,588 nT.
All formulas presented here are valid for geographical angles (North = 0° = 360°, East = 90°, South = 180°, and West = 270°) but have to be modified if
mathematical angles are used (East = 0°, North = 90°, West = 180°, and South = 270°). What should the same magnetometer read on X and Y if the same
geomagnetic field is turned horizontally to 165°?#
# X = −17,387 nT; Y = +4659 nT.

117Chapter | 8 Magnetoreception in Birds and Its Use for Long-Distance Migration
small bird with a 2 cm wide head to determine from which
direction infrasound originates (Mouritsen, 2013).
Thus, the primary orientation system of young inexpe-
rienced migrants on their first autumn migration is likely to
be based primarily on celestial and magnetic cues, and it is
known that when first-time autumn migrants are displaced
away from their migration route, they are unable to correct
for displacements (Drost, 1938; Perdeck, 1958; Mouritsen
and Larsen, 1998; Mouritsen, 2003; Thorup et al., 2007;
Holland, in press). Instead, they choose a migration route
parallel to their normal route; thus, they do not seem to
possess a map sense (see Figure 8.3). The migratory pro-
gram of first-season solitary migrants can be described
as a “clock-and-compass,” “calendar-and-compass,” or
“vector navigation” strategy (Mayr, 1952; Perdeck, 1958;
Schmidt-Koenig, 1965; Rabøl, 1978; Berthold, 1991;
Mouritsen, 1998b; Mouritsen and Mouritsen, 2000;
Mouritsen, 2003) in which the birds fly in a specific
direction for a given amount of time independent of their
present location. Because the system includes little (see
below under magnetic signposts) or no location-related
feedback, the orientation strategy of first-time solitary
migrants can be mathematically described as a directed ran-
dom walk: The birds choose their flight direction randomly
from a normal-like distribution pointing in their mean
migratory direction each evening independent of previous
events (Mouritsen, 1998b; Mouritsen and Mouritsen, 2000;
Mouritsen et al., 2013). This strategy predicts that the
statistical distribution of first-time migrants should be
parabolic, and it has been shown that this prediction fits
very well with the actual distribution of ringing recover-
ies of free-flying, first-time migrants in Western Europe
(Mouritsen, 1998b; Mouritsen and Mouritsen, 2000).
The orientation task facing adult migrants and young
migrants on their first spring migration is fundamentally
different from the task faced during their first autumn
migration (Kramer, 1957; Rabøl, 1978; Berthold, 1991;
Mouritsen, 2003; Holland, in press). Adult migrants and
young migrants on their first spring migration are migrating
back toward a region with which they have had previous
experience; therefore, their orientation system is likely to
include local (map) information gained through previous
migration experience. Birds that would use sensory infor-
mation from all useful senses, which would improve their
90
180
270
gN
90
180
270
gN
$ %
DE F
IGH
FIGURE 8.3 Displacement experiments provide key evidence for understanding the spatiotemporal orientation strategies of migratory birds.
(A) Perdeck’s classical experiments in which he displaced >10,000 starlings from Holland S/SSE (→) to Switzerland during autumn migration showed
that young starlings (•) on their first autumn migration were unable to correct for the displacement. The young birds show a parallel displaced migration
pattern relative to the wintering area of nondisplaced controls (dashed area) whereas adult starlings (Δ) orient directly back to the normal population-
specific wintering area of nondisplaced controls (From Mouritsen (2003) after Schmidt-Koenig (1965); Perdeck (1958)). (B) Displacement experiments,
in which Eurasian Reed Warblers (Acrocephalus scirpaceus) were tested in Emlen funnels (Emlen and Emlen, 1966; Mouritsen et al., 2009) before and
after displacement, showed that young birds on their first spring migration are already able to correct for 1000-km eastward displacements to a location
where they have certainly never been before (b). (a) Orientation of birds at the capture site (Rybachy). (c) Orientation of the same birds after the 1000 km
eastward translocation to Zvenigorod. Each dot at the circular diagram periphery indicates the mean orientation of one individual bird. The arrows show
group mean directions and vector lengths. The dashed circles indicate the length of the group mean vector needed for significance according to the
Rayleigh test (5% and 1% level for inner and outer dashed circles, respectively). The lines flanking group mean vectors indicate the 95% confidence inter-
vals for the mean direction. gN = geographic North. On (b), a map of the displacement region is shown. The shaded light-gray zone represents the breeding
range of Eurasian Reed Warblers and the dashed arrows show the expected results in case of (1) no compensation for the displacement or (2) compensa-
tion toward the eastern part of the breeding range. Notice that intact birds compensate for the displacement whereas birds that had the ophthalmic branch
of the trigeminal nerve cut (d–f) could no longer compensate for the displacement. Re-assembled after Chernetsov et al. (2008); Kishkinev et al. (2013).

PART | II Sensory Biology and Nervous System Theme
118
ability to find their way (e.g., magnetic sense, olfaction,
vision, and hearing), should have an evolutionary advan-
tage over birds that would only use a single cue or sense.
Thus, it is likely that the orientation strategies of experi-
enced migrants are multisensory and involve learned maps
(Mouritsen, 2003, 2013; Holland, in press). Indeed, in con-
trast to first-time migrants, experienced migrants are able to
correct for displacements (Perdeck, 1958; Mewaldt, 1964;
Thorup et al., 2007; Chernetsov et al., 2008; Kishkinev
et al., 2010, 2013) and thus have added a learned map to
their orientation program (see Figure 8.3). Interestingly,
this map is also functional at locations that have not been
visited previously: Birds can appropriately correct their
orientation when they are experimentally displaced to far-
away locations where they have certainly never been before
(Perdeck, 1958; Mewaldt, 1964; Thorup et al., 2007; Cher-
netsov et al., 2008; Kishkinev et al., 2010, 2013). If their
learned map would have been based exclusively on previ-
ously experienced local landmarks, then it should not have
worked at unfamiliar locations. Although the functional
basis of this map sense is not yet understood (Holland, in
press), it is almost certainly based on multiple cues and it
must involve the detection of larger scale gradients, which
can be extrapolated and thus enable birds to return from
unfamiliar locations.
8.6 THE MAGNETIC COMPASS OF BIRDS
Friedrich W. Merkel and Wolfgang Wiltschko discovered
that birds have a magnetic compass sense in the mid-1960s
(Merkel and Wiltschko, 1965; Wiltschko, 1968). When
birds are placed in a round cage at night, they show migra-
tory restlessness (or Zugunruhe in German, Kramer, 1949):
The birds primarily jump/flutter in their migratory direc-
tion, and when the magnetic field is turned horizontally in
the absence of celestial cues, the birds turn their orientation
with the magnetic field (see Figure 8.4). This is the behav-
ioral evidence required to show that a migratory bird species
possesses and is able to use a magnetic compass (Wiltschko
and Wiltschko, 1995). A magnetic compass has been found
in more or less every migratory bird species properly tested
for it (Wiltschko and Wiltschko, 1995); therefore, it is quite
safe to presume that all migratory birds and potentially
birds in general possess a magnetic compass.
It is important to note that there are at least two dif-
ferent magnetic field properties that could potentially
N
(A) (B)
N
S
E
W
S
N
N
S
E
W
S
N
N
S
E
W
S
N
NS
E
W
S
N
N
S
E
W
S
N
?
FIGURE 8.4 The Emlen funnel and the inclination compass. (A) The so-called Emlen funnel is the most commonly used orientation cage (Emlen
and Emlen, 1966). The mean jumping direction of the birds are recorded on scratch-sensitive paper lining the inclined wall of the funnel (Mouritsen et al.,
2009). (B) Early experiments by Wiltschko and Wiltschko (1972) have shown that birds have an inclination compass, which means that the birds measure
the angle between the magnetic field lines and the Earth’s surface or gravity; thereby, the birds separate between poleward and equatorward, not between
North and South like a polarity compass would do (if birds use a polarity compass, then they should have oriented in the direction indicated by the red end
of the inserted technical compass). Birds are disoriented in a horizontal magnetic field like the one occurring at the magnetic equator. The flight direction
of the inserted bird indicates the springtime mean direction chosen by all bird species tested so far in the given magnetic field (Wiltschko and Wiltschko,
1995). The red arrows indicate the direction if the magnetic field lines. Brown bar = the Earth’s surface, N = geographic North, S = geographic South.
Figure and legend is reused from Mouritsen (2013).

119Chapter | 8 Magnetoreception in Birds and Its Use for Long-Distance Migration
be used as input for a magnetic compass sense. A mag-
netic polarity compass (e.g., the human ship compass)
uses only the horizontal component of the field lines,
which points toward Magnetic North anywhere on Earth
except at the magnetic poles. On the other hand, a mag-
netic inclination compass detects only the angle between
the geomagnetic field lines and the Earth’s surface or
gravity—not the polarity of the field lines. The smallest
angle between the Earth’s surface and the geomagnetic
field lines indicates the direction “toward the magnetic
equator” whereas the greatest angle indicates “toward
the magnetic pole.” Because the inclination is opposite
on the Northern and Southern Hemisphere, respectively,
this holds on both hemispheres. All bird species prop-
erly tested so far have a magnetic inclination compass
(Wiltschko and Wiltschko, 1972, 1995; see Figure 8.4).
Thus, the magnetic compass of night-migratory birds
does not separate between North and South like our
ship compass, but it distinguishes between “toward the
magnetic equator” and “toward the magnetic pole” (the
Magnetic North Pole in the Northern Hemisphere and the
Magnetic South Pole in the Southern Hemisphere). Fur-
thermore, the birds’ magnetic compass sense seems to
have a rather narrow functional intensity window, but this
window seems to be extendable to new intensities after
a few hours of adaptation to a changed magnetic field
intensity (Wiltschko, 1978).
8.7 DO BIRDS POSSESS A MAGNETIC MAP?
Many studies have reported that magnetic cues play an
important role in birds’ sense of position (i.e., that birds have
a “magnetic map”). However, the existence of a magnetic
map is heavily debated, and the views among researchers
range from a magnetic map with a precision of a few kilo-
meters being an established fact (Walcott, 1991; Wiltschko
and Wiltschko, 1995; Wiltschko et al., 2010a) to a magnetic
map sense being an evergreen phantom (Wallraff, 2001;
Gagliardo et al., 2009). One thing is for sure; the natural map
sense of birds is multifactorial. It relies on input from olfac-
tion (Papi, 1991; Wallraff, 2001, 2005; Gagliardo et al., 2006,
2008, 2009) and vision (Guilford et al., 2004) and possibly
also from magnetic sensing (Dennis et al., 2007; Holland,
2010; Kishkinev et al., 2013) and maybe even from hearing
(Hagstrum, 2013 but see Wallraff, 1972; Holland, in press).
Pigeons with opaque lenses that prevented them
from detecting any local visual landmarks can return to
within c. 5 km of their loft (Schmidt-Koenig and Walcott,
1978). Thus, the precision of nonlandmark-based navi-
gation seems to be a few kilometers, but which cue(s)
enable pigeons to home to within c. 5 km of their loft
without being able to use visual landmarks? At pres-
ent, informed neutral observers of the olfaction contra
magnetic map controversy agree (Able, 1996; Mouritsen,
2013; both are orientation researchers who have never
performed a pigeon release; thus, they have no vested
interest in any of the camps) that the evidence suggest-
ing that chemical cues (odors) play an important role in
the nonlandmark-based part of pigeons’ map sense (Papi,
1991; Wallraff and Andreae, 2000; Wallraff, 2001, 2005;
Gagliardo et al., 2006, 2008, 2009) is much more con-
vincing than the evidence supporting an important role
of magnetic cues in the pigeons’ map (e.g., Walcott,
1991; Wiltschko and Wiltschko, 1995; Dennis et al.,
2007; Wiltschko et al., 2010a; Holland, 2010). However,
remember that in the end, both camps may be right. The
map will be multifactorial because a bird using all avail-
able input from all of its senses will have an evolutionary
advantage over a bird using only a single cue for a task so
essential for the survival of a bird. In any case, it remains
very difficult to understand how a magnetic-field-based
map sense should be able to function on a scale less than
10 km. Why is that?
The problem for a bird wanting to use a magnetic map
is that the average change in magnetic field intensity is only
c. 3 nT/km on the North-South axis: The geomagnetic field
changes c. 30,000 nT from one of the magnetic poles to the
magnetic equator, which are c. 10,000 km apart. Likewise,
magnetic inclination changes only c. 0.009°/km along the
North-South axis (a 90° change over 10,000 km). On the
East-West axis, there is generally very little change in mag-
netic field intensity and magnetic inclination. Thus, any
magnetic-field-based input to a reasonably precise map
would require a very accurate magnetic sensory system and
a very accurate sense of gravity. However, even if birds have
such a system, daily, partly stochastic, natural variations in
the geomagnetic field on the order of 30–100 nT in more
or less random directions mean that it is very difficult to
imagine how a magnetic-field-based map sense could have
a precision less than 10–30 km (during magnetic storms
generated primarily by the Sun, the geomagnetic field vari-
ability can reach 1000 nT; Courtillot and Le Mouël, 1988).
Therefore, it is possible that magnetic parameters may only
help determine position where the expected differences in
the magnetic field parameters are consistently larger than
the daily magnetic variations (Mouritsen, 2013).
Other cues such as odors and familiar landmarks may
be more significant map parameters at shorter distances. It
is much easier to imagine that a magnetic map could be
relevant on a much larger spatial scale, and intriguing data
exist that suggest that some songbirds can use magnetic
cues as an approximate geographic “signpost”, which, for
example, tells the birds when to increase their fat reserves
before crossing the Sahara Desert (Fransson et al., 2001) or
when to change their migratory heading (Henshaw et al.,
2010). This case, in which specific magnetic parameters
trigger a change in behavior, is referred to as a magnetic
signpost (Mouritsen, 2013).

PART | II Sensory Biology and Nervous System Theme
120
8.8 INTERACTIONS WITH OTHER CUES
In most orientation-related contexts, magnetic cues inter-
act with several other sources of similar and/or conflict-
ing information. For instance, night-migratory songbirds
not only have a magnetic compass, they also have a Sun
compass and a star compass (Emlen, 1975; Schmidt-König
et al., 1991; Mouritsen and Larsen, 2001; Cochran et al.,
2004; Zapka et al., 2009). They only need information
from any one of these compasses to orient in the appro-
priate direction (Mouritsen, 1998a; Muheim et al., 2006b;
Chernetsov et al., 2011; Liu and Chernetsov, 2012). If the
three compasses provide conflicting information, then it is
not consistent which compass the birds prefer. The prefer-
ence is probably dependent on the ecological context, the
details of the experimental setup, and the conditions under
which the birds were housed and tested, and it is likely that
various calibrations are taking place in nature (see Figure 8.5,
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FIGURE 8.5 Some birds calibrate their magnetic compass from celestial cues around sunset. Tracks of free-flying Gray-Cheeked Thrushes (A) and
Swainson’s Thrushes (B) released from Champaign, Illinois, are shown. The arrows indicate the direction and ground tracks of migratory flights when wind
effects were discarded. Black arrows indicate migratory flights of nonmanipulated individuals. Red arrows indicate migratory flights of experimental birds
that had experienced a magnetic field turned to 80° East before takeoff, and yellow arrows indicate the migratory flights of the experimental birds during sub-
sequent nights. White arrows indicate the migratory flight paths of experimental birds that did not migrate on the night of magnetic treatment, but they did so
1–6 days later. Connected arrows show flights of the same individual during successive nights. Data are depicted differently in (A) and (B) because for Grey-
Cheeked Thrushes, experimental and control birds are different individuals whereas in Swainson’s Thrushes, the same experimental individuals were followed
for at least two successive nocturnal migrations (because of the large spread in natural headings). Broken lines indicate that birds were lost during tracking at
the site where the broken lines start. Notice that the birds that experienced a magnetic field turned 80° to the East during sunset and that were released after
all light from the Sun had disappeared migrated toward the West when they embarked on migration on the same night. On later nights, they migrated in the
appropriate northerly spring migratory direction. These results mean that the birds had calibrated their magnetic compass from their Sun compass before take-
off and that this calibration happens daily. The reasons are illustrated in (C–F): (C) For control birds all cues gives the same information. (D) If experimental
birds calibrate their magnetic compass from sunset-related cues, they will calibrate their magnetic compass so that 80° counter-clockwise to the magnetic
field lines will be their “North” for the coming night. (E) After release, the experimental birds experience the natural field lines. Because all light from the
Sun has disappeared, no new calibration is possible at time of release and their wrongly sunset-calibrated magnetic compass makes them fly 80° counter-
clockwise relative to the natural field lines, which is towards the west for the rest of the first night. (F) On then second night after release, Sun and magnetic
cues are in agreement and the birds will reorient into their intended migratory direction. The four thin parallel arrows (C–F) indicate the horizontal direction
of the magnetic field lines experienced by the birds. The thick arrow indicates the expected orientation of the birds. The setting Sun and the three lines with
double arrowheads indicate whether Sun and polarized light cues were available for calibration. Figure and parts of the legend from Cochran et al. (2004).

121Chapter | 8 Magnetoreception in Birds and Its Use for Long-Distance Migration
Cochran et al., 2004; Muheim et al., 2006a; Liu and
Chernetsov, 2012). The only experiment with truly free-
flying birds performed so far suggested that two species of
North-American songbirds used the magnetic compass as
their primary compass in midair during spring migration, but
that they calibrate this compass on the basis of celestial cues
during the sunset period (Cochran et al., 2004); however,
this mechanism is not universal (Chernetsov et al., 2011).
Other evidence suggests that polarized light cues might be
crucial for this calibration (Muheim et al., 2006a); how-
ever, so far, it is not understood how a bird’s eyes can detect
polarized light.
In pigeon homing or any other map-related task, the
interactions between different cues seem to be even more
complicated. Homing pigeons have been shown to use
olfactory cues (Papi, 1991; Wallraff and Andreae, 2000;
Wallraff, 2001, 2005; Gagliardo et al., 2006, 2008, 2009),
visual landmarks of various kinds (Guilford et al., 2004),
outward journey information (reviews in Wiltschko and
Wiltschko, 1995; Wallraff, 2005), and maybe magnetic
cues (Walcott, 1991; Wiltschko and Wiltschko, 1995;
Dennis et al., 2007; Wiltschko et al., 2010a) to estimate their
position relative to home when released from a previously
unknown location. The relative importance of these map
cues is hotly debated, with many apparently contradictory
results occurring in the literature. One reason may very well
be that in one location, one type of cue may be particularly
reliable whereas another cue is more reliable in a differ-
ent location; therefore, the animals predominantly rely on
different cues in different locations. The most convincing
experiments performed to date involved cutting of the olfac-
tory nerves or cutting of the ophthalmic branch of the tri-
geminal nerves in experienced and inexperienced pigeons.
The experiments showed that homing pigeons tested around
Pisa in Italy need intact olfactory nerves but not intact
“magnetic” nerves (see Section 8.9) to home (Gagliardo
et al., 2006, 2008, 2009). In procellariiform seabirds such
as albatrosses and shearwaters, olfactory cues also seem
to be much more important for navigation than magnetic
cues (Mouritsen et al., 2003; Nevitt and Bonadonna, 2005;
Bonadonna et al., 2005; Gagliardo et al., 2013).
8.9 HOW DO BIRDS SENSE THE EARTH’S
MAGNETIC FIELD?
It is challenging to detect the weak geomagnetic field with
biological materials. Considering the anatomical constraints
and known structures found within small birds, careful
models of putative sensory mechanisms often find it hard
to explain how a 50,000 nT magnetic field can result in reli-
able signals in the presence of thermal fluctuations (kT) and
other sources of noise. In fact, any biological mechanism
that can, in principle, allow detection of 50,000 nT fields is
noteworthy (Ritz et al., 2010; Mouritsen, 2013). Only three
basic mechanisms are currently considered to be physically
viable: (1) induction in highly sensitive electric sensors, (2)
iron-mineral-based magnetoreception, and (3) radical-pair
based magnetoreception.
8.10 THE INDUCTION HYPOTHESIS
Electromagnetic induction is the production of voltage
across an electric conductor situated in a changing magnetic
field or a conductor moving through a stationary magnetic
field. Thus, in practical terms, if one has an electric wire
and one moves this through a magnetic field, then a current
will be generated in the wire. If this wire is ring or coil-
shaped, directional sensitivity can be achieved. In biological
tissues, one would need conductive, liquid-filled, ring-like
structures of sufficient size and diameter to generate mea-
surable electrical signals that can be picked up by an electri-
cally sensitive receptor cell. For electromagnetic induction,
Lorenzini ampullae are a concrete realization of an electri-
cally sensitive cell operating in saltwater fish (von der Emde,
2013). Their function uses the fact that saltwater is electri-
cally conductive, and aquatic animals could potentially use
induction to sense the geomagnetic field (Kalmijn, 1981;
Molteno and Kennedy, 2009). However, no strong evidence
currently exists that fish actually use their electric sense to
deduce information from the geomagnetic field (Kirschvink
et al., 2010; Mouritsen, 2013). In land-based animals, it is
difficult to imagine how induction could be used to sense the
geomagnetic field because air has low conductivity; there-
fore, the needed structures would have to be realized inside
of the animals themselves. In fact, biophysical consider-
ations effectively eliminate induction as a potential source
of magnetodetection in terrestrial animals: The required
physiological structures filled with conductive liquid would
be large and easily detectable, but no such structures have
been reported (Kirschvink et al., 2010; Mouritsen, 2013).
Thus, for terrestrial animals such as birds, another mecha-
nism must be responsible for magnetoreception.
8.11 THE IRON-MINERAL-BASED
HYPOTHESIS
When human beings want to use the direction of the geomag-
netic field for orientation, we use a technical compass that
is based on a needle made of magnetized iron or a magnetic
iron compound that moves in the horizontal plane. There-
fore, the first suggestion almost any human thinks of when
one asks them how birds may detect the geomagnetic field is
“Maybe they have little compass needles in their head.” It is
not surprising that this suggestion was also the first sugges-
tion scientists came up with. A compass needle-like struc-
ture has been realized inside of magnetotactic bacteria (see
Figure 8.6(A), Blakemore, 1975; Frankel and Blakemore,
1989). A chain of single-domain magnetite crystals
( Blakemore, 1975; Frankel and Blakemore, 1989; Kirschvink
et al., 2010) or other very similar iron oxides (Falkenberg

PART | II Sensory Biology and Nervous System Theme
122
et al., 2010) would be the easiest realization of a small
compass-needle-like structure inside of a bird, but other
arrangements of iron-mineral crystals could also work as
a magnetic field detector (Solov’yov and Greiner, 2009;
Kirschvink et al., 2010). The iron-mineral crystals are
expected to transduce the magnetic signal by opening
or closing pressure-sensitive ion channels (Johnsen and
Lohmann, 2005).
Many studies have documented the presence of mag-
netite or some other kind of iron mineral crystals in
almost any animal, in which researchers have seriously
looked for such crystals (e.g., in Caenorhabditis elegans,
mollusks, insects, crustaceans, and various vertebrates;
Mouritsen, 2013). However, the mere existence of iron
mineral crystals or even magnetite does not represent sig-
nificant evidence by itself that such structures have any
relevance to magnetoreception (Mouritsen, 2013). Iron
is an important element required for proper function of
most organisms. Consequently, iron homeostasis is impor-
tant, and iron mineral deposits may just be a way for an
organism to get rid of excess iron. Therefore, only if iron
mineral structures are found at consistent, specific loca-
tions and are associated with the nervous system do the
iron mineral structures qualify as serious magnetosensory
candidate structures (Mouritsen, 2013). The existence of
magnetite crystal chains, which lead to a magnetically ori-
ented swimming behavior in so-called “magnetotactic bac-
teria” (Blakemore, 1975; Frankel and Blakemore, 1989;
Bazylinski and Frankel, 2004), unequivocally proves that
living cells can, in principle, synthesize magnetite that will
align with the geomagnetic field. However, the magnetite
crystals in these bacteria are not part of an active sensory
system; they only lead to passive alignment (Wiltschko and
Wiltschko, 1995; Mouritsen, 2013).
Magnetite spherules
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FIGURE 8.6 Iron-mineral structures in birds. (A) Transmission electron micrograph of the magnetotactic bacteria, Magnetospirillum magnetotacti-
cum, showing the magnetosome chain inside of the cell. Scale bar: 1 μm (Photograph © Richard B. Frankel). Magnetosomes would be the most straight-
forward solution for a magnetic field sensor in the nervous system of a bird, but, so far, magnetosomes have not been proven to occur in any bird. (B) Bird
head schematically illustrating the anatomical location of the three branches of the trigeminal nerve. (C) Schematic drawing of iron mineral-containing
structures in birds’ upper beak illustrating the opposing interpretations of Fleissner et al. (2003) and Treiber et al. (2012). Part (C) reproduced with permis-
sion from Mouritsen (2012), (B) and panel composition is reproduced from Mouritsen (2013).

123Chapter | 8 Magnetoreception in Birds and Its Use for Long-Distance Migration
The currently most promising, but not proven, active, iron-
mineral-based magnetoreceptor candidate structures are those
reported from the olfactory epithelium of fish (Walker et al.,
1997; Eder et al., 2012). Elaborate iron-mineral-based struc-
tures thought to be magnetoreceptors have also been reported
in the upper beak of birds (Fleissner et al., 2003; Falkenberg
et al., 2010). However, recent findings suggest that these struc-
tures are macrophages involved in iron homeostasis (Treiber
et al., 2012). Thus, at present, no convincingly documented,
iron-mineral-based, magnetoreceptive candidate structures are
known from birds (see Figure 8.6(C); Mouritsen, 2012).
Conditioning of birds to magnetic stimuli has also proven
to be very difficult, and independent replication is rare. It
has been reported that homing pigeons, Colomba livia, can
be conditioned to respond to strong magnetic fields (Mora
et al., 2004; Mora and Bingman, 2013). The conditioned
response to a very strong magnetic field (c. 2 times the
strength of the geomagnetic field) required intact trigeminal
nerves (Mora et al., 2004). Consequently, pigeons seem to,
in principle, be able to detect strong magnetic field changes
via the ophthalmic branch of the trigeminal nerve. However,
to use geomagnetic information for a map, animals must be
sensitive to changes in the geomagnetic field, which are 3–5
orders of magnitude smaller than the anomalies used in the
successful conditioning experiments. Using a very similar
paradigm adapted for European robins and using weaker
fields resulted in nicely conditioned responses to auditory
stimuli but failed to produce a conditioned response to mag-
netic field stimuli (Kishkinev et al., 2012).
The ophthalmic branch of the trigeminal nerve (see
Figure 8.6(B)) terminates in the principal (PrV) and spi-
nal tract (SpV) nuclei of the trigeminal brainstem complex
(Williams and Wild, 2001; Heyers et al., 2010; see Figure 8.7).
Recent evidence shows that subpopulations of neurons in
PrV and SpV in European robins (Erithacus rubecula),
a night-migrating songbird, are activated by changing
(A)
(C) (D) (E)
(F)
(B)
FIGURE 8.7 There are magnetically activated neurons in the two hindbrain regions, PrV and SpV, which receive sensory input from the ophthal-
mic branch of the trigeminal nerve (V1) in birds. (A) Anatomical overview of the termination of the trigeminal nerve in the avian hindbrain. (B–F) In birds
with intact V1 (sham-sectioned nerves; (D)), stimulation with a changing magnetic field (CMF) leads to increased expression of the neuronal activity-depen-
dent gene, ZENK (black dots in (D–F) are activated neuronal nuclei), in the hindbrain regions (PrV, shown in (C–F)) and SpV, that receive their primary input
from the trigeminal nerve. This activation disappears when the magnetic field stimulus is absent (ZMF = zero magnetic field; (E)). The activation also disap-
pears when the CMF is present but the birds had V1 bilaterally sectioned (CMF Sect; (F)). No magnetic field-dependent activation is seen in control regions
such as the optic tectum (B). (C) Acetyl cholinesterase (AChE) is a good anatomical marker for identification of the borders of PrV. From Heyers et al. (2010).

PART | II Sensory Biology and Nervous System Theme
124
magnetic field stimuli but not by a zero magnetic field
(Heyers et al., 2010). Furthermore, the activation in the chang-
ing magnetic field disappears when the ophthalmic branch
of the trigeminal nerve is severed (see Figure 8.7(B–F)).
These findings suggest that the ophthalmic branches of
the trigeminal nerves carry magnetic information in birds
(Heyers et al., 2010). However, the sensory origin (most
likely iron-mineral-based) and the biological significance
of the trigeminally mediated magnetic information are
unclear at present (Mouritsen, 2012, see Figure 8.6(C)).
Information from the ophthalmic branch of the trigeminal
nerve is neither required nor sufficient for magnetic com-
pass orientation in several night-migrating songbird species
(Zapka et al., 2009, see Figure 8.8). Homing experiments
with pigeons have shown that pigeons tested around Pisa,
Italy, need intact olfactory nerves but not intact trigeminal
nerves to home (Gagliardo et al., 2006, 2008, 2009).
The most likely function of the trigeminal nerve-
related magnetic sense is to detect large-scale changes
in magnetic field strength and/or magnetic inclination,
which could be used to determine approximate position.
A very recent set of experiments has shown that Eurasian
Reed Warblers, Acrocephalus scirpaceus, are capa-
ble of correcting for a 1000 km eastward displacement
(Chernetsov et al., 2008), but that this ability disappears
when the ophthalmic branch of the trigeminal nerve is
cut (Kishkinev et al., 2013, see Figure 8.3). In addition,
experiments with night-migratory songbirds exposed to
strong magnetic pulses, which are thought to disturb any
magnetite-based magnetic sense for days to weeks but
should not have any effect after the treatment itself on a
light-dependent magnetoreception mechanism, support
the idea that the magnetic map or signpost sense is iron
mineral-based (Wiltschko et al., 2009; Holland, 2010;
Holland and Helm, 2013).
It has also very recently been suggested that the avian
lagena (a part of the birds’ vestibular system) plays a role in
magnetodetection (Wu and Dickman, 2011, 2012). Whether
the lagena provides the primary magnetic information or
gravity information to the magnetic sense is not yet clear, but
if the seemingly very convincing electrophysiological data
(Wu and Dickman, 2012) can be independently replicated,
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were performed on European robins, Erithacus rubecula (Photo © Henrik Mouritsen). The reference direction provided by the Earth’s magnetic field is
detected in the birds’ eyes, where cryptochrome proteins are the most likely light-dependent magnetic sensory molecules. Light absorption is thought to
generate long-lived flavin-tryptophan radical pairs within cryptochromes in the retina, the reaction yields of which are determined by the orientation of
the molecule with respect to the geomagnetic field vector. If the cryptochromes were associated e.g. with the membrane disks of the outer segments of the
photoreceptors, then an ordered structure could result, and different reaction yields in different parts of the retina could be compared to provide a visual
impression of the compass bearing (see Figure 8.9). Light-dependent magnetic compass information is transmitted from the retina through the optic nerve
to the visual thalamus and from there to Cluster N in the forebrain via the thalamofugal visual pathway (Figure 8.11). If Cluster N is destroyed, European
robins can no longer use their magnetic compass (Figure 8.12). The illustration of the cryptochromes bound to photoreceptor membranes is modified from
Solov’yov et al. (2010). The reaction scheme is modified from Rodgers and Hore (2009). Figure and parts of the legend from Mouritsen and Hore (2012).

125Chapter | 8 Magnetoreception in Birds and Its Use for Long-Distance Migration
then the role of the lagena in magnetoreception is very sig-
nificant indeed, and the vestibular brainstem nuclei would
be a very important processing station for magnetic field
information.
8.12 THE LIGHT-DEPENDENT HYPOTHESIS
The magnetic compass behavior of newts (Phillips and
Borland, 1992) and birds (Wiltschko et al., 1993; Muheim
et al., 2002; Wiltschko et al., 2010b) is dependent on the
wavelengths of light being available during behavioral tests.
Already in the late 1970s, theoretical considerations led
Klaus Schulten to suggest that chemical reactions in pho-
tosensitive molecules could form the basis of a magnetic
compass sense (Schulten et al., 1978).
The principles of the suggested light-dependent mag-
netic sensing mechanism are illustrated in Figure 8.8. A
light-sensitive molecule (D) absorbs light and uses the light
energy to transfer an electron to an acceptor (A); thereby,
a radical pair is produced. If this radical pair is long-lived
(>1 μs), then it can, depending on the spin of the electrons,
exist in one of two states—a singlet state (spins antiparallel)
or a triplet state (spins parallel). It is known from chemistry
that singlet and triplet states have different chemical proper-
ties; thus, they often result in different chemical end prod-
ucts. Earth-strength magnetic fields can theoretically affect
this statistical equilibrium and thereby modulate a presently
unknown biochemical pathway (Schulten et al., 1978; Ritz
et al., 2000, 2010; Rodgers and Hore, 2009; Hore, 2012).
How can we imagine that a bird using a light-induced,
radical-pair mechanism would detect the magnetic field? It
is possible that a virtual visual image would literally enable
birds to “see” the direction of the magnetic field lines (e.g.,
Ritz et al., 2000, 2010; Solov’yov et al., 2010). If one makes
the simple assumption that the sensory molecules are ori-
ented perpendicularly to the eyeball (see Figure 8.9), then
the half ball shape of the retina would mean that molecules
oriented in all axial directions would occur (Ritz et al., 2000;
Mouritsen, 2013). If a bird looks in the direction of the mag-
netic field lines, then in the line of sight, the retinal mol-
ecules would be parallel to the magnetic field and this could
lead to a light pixel. At the edge of the eye, the molecules
would be perpendicular to the magnetic field, and this could
lead to darker pixels. In between, the molecules would be
oriented at different angles relative to the magnetic field,
and various shades of gray pixels could appear. Altogether,
this could lead to a virtual image looking somewhat like
the one shown to the right in Figure 8.9 (Ritz et al., 2000;
Mouritsen, 2013). This pattern is only for illustrative pur-
poses of the principle. We have much too little information
available at present to know what an actual magnetically
modulated light pattern seen by a bird would look like
(Mouritsen, 2013). The patterns might become easier to
see when they move across the retina during so-called head
scan behavior (Mouritsen et al., 2004b; Ritz et al., 2010).
If the radical-pair mechanism is responsible for magneto-
reception, then it means that it is based on a quantum mechan-
ical effect (Rodgers and Hore, 2009; Ball, 2011; Mouritsen
and Hore, 2012; Hore, 2012; Hogben et al., 2012; Solov’yov
et al., 2014; Engels et al., 2014). In fact, it might be the only
sensory mechanism in biology to be inherently quantum in
nature. Critics of the radical-pair mechanism have pointed
out that the interaction energy between a geomagnetic field
and a radical is typically several orders of magnitude below
the background thermal energy, kBT (Kirschvink et al., 2010).
At first glance this might seem like a problem, but because
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FIGURE 8.9 How the light-dependent, radical pair-based, magnetic sensing mechanism could lead to perception of a visual image. Principal
illustration suggesting how birds could, in principle, convert a magnetic stimulus into a putative visual image. Left: 3D illustration of the half-sphere of
an eyeball. Red pins simulate cryptochrome orientation all pointing toward the center of the eyeball. If a bird would be looking in the direction of the
magnetic field lines, one could imagine that the bird would see a pattern similar to the one illustrated on the right because the light sensitivity of one or
more cryptochromes would depend on their orientation relative to the axis of the magnetic field lines. Redrawn after Mouritsen (2013) inspired by Ritz
et al. (2000).

PART | II Sensory Biology and Nervous System Theme
126
the spins are not in equilibrium, this is not a fundamental
problem. Very weak magnetic interactions can essentially
affect radical pair reactions for three reasons (Hore, 2011):
(1) radical pair chemistry is controlled by the electron spins
in the radicals, (2) the electron spins are not at thermal equi-
librium, and (3) the electron spins behave quantum mechani-
cally. Weak magnetic fields affect the coherent behavior of
the electron spins in a fundamentally quantum manner in
which kBT plays no role. Instead of comparing interaction
energies to kBT, one must compare the time required for a
magnetic interaction to have an effect with the time required
for the system to reach thermal equilibrium (Hore, 2011). If
the former is shorter than the latter, then the magnetic field
can have an effect (Hore, 2011). As an excellent analogy
(Hore, 2011), one can imagine a fly and a rectangular granite
block. If the granite block is standing on one of its sides (con-
ventional physics, equilibrium), then the fly has no chance
to flip the granite block, but if the granite block is balancing
on one of its corners (quantum mechanics, nonequilibrium),
then, depending on where the fly lands, it might flip the gran-
ite block to one or the other side (Figure 8.10).
Which molecule can be responsible for light-dependent
magnetoreception? Opsins cannot function as radical- pair-
based magnetoreceptors because opsins use the light energy
to change a chemical bond, not to transfer an electron. The
only currently known photoreceptor molecules found in ver-
tebrates that can use light energy to form long-lived radical
pairs are the cryptochromes (Ahmad and Cashmore, 1993;
Cashmore et al., 1999; Ritz et al., 2000, 2010; Giovani et al.,
2003; Liedvogel et al., 2007a; Biskup et al., 2009; Rodgers
and Hore, 2009; Liedvogel and Mouritsen, 2010). Some
cryptochromes are known to be involved in circadian clocks
(Cashmore et al., 1999; Sancar, 2003). However, in birds,
more cryptochromes than the ones thought to be involved in
the clock occur; therefore, it is easy to imagine that they can
play a role in other biochemical processes (Liedvogel and
Mouritsen, 2010). Cryptochromes are related to the DNA
repair enzymes called photolyases (Cashmore et al., 1999;
Sancar, 2003) and consist of a photolyase homology region
and a C-terminal end, which varies greatly between differ-
ent cryptochromes (Cashmore et al., 1999; Sancar, 2003;
Müller and Carell, 2009; Liedvogel and Mouritsen, 2010).
The C-terminal is thought to be involved in binding crypto-
chromes to currently unknown interaction partners (Sancar,
2003; Liedvogel and Mouritsen, 2010; Mouritsen and Hore,
2012). Cryptochromes noncovalently bind the cofactor fla-
vin. The light-induced electron transfer is thought to take
place between the flavin and three tryptophane residues
within the cryptochrome protein (Gindt et al., 1999; Biskup
et al., 2009; Rodgers and Hore, 2009; Solov’yov et al., 2012).
FIGURE 8.10 Granite block analogy of light-dependent magnetoreception. A granite block analogy can help understand how a radical pair-based
mechanism can theoretically be used to sense Earth-strength magnetic fields, although the energy exerted by the magnetic field on the radical is much
lower than thermal energy, kBT. Imagine a granite block standing on one of its sides. If a fly lands on the granite block while it is in this position, then
there is no way the fly can make the granite block flip over. In fact, quite a lot of energy is needed to move the granite block onto one of its corners, but
once it is on one of its corners, a very small amount of energy can influence which way the granite block falls. Now, even a fly landing on the granite
block may make it flip over to one or the other side. In the light-dependent, radical pair-based magnetoreception hypothesis, light has much more energy
than the magnetic field. It is the absorption of light that brings a photoreceptor molecule (probably a cryptochrome) into an exited state (moves the granite
block onto its corner in the analogy), which is then highly sensitive to even very small magnetic field effects (the fly landing onto the granite block in the
analogy). After Hore (2011).

127Chapter | 8 Magnetoreception in Birds and Its Use for Long-Distance Migration
Cryptochromes are predominantly found within photorecep-
tor cells and ganglion cells in the eyes of birds (Mouritsen
et al., 2004a; Möller et al., 2004; Niessner et al., 2011), and
cryptochromes are currently the only seriously considered
candidate molecules for radical-pair-based magnetorecep-
tion in birds (Mouritsen and Ritz, 2005; Rodgers and Hore,
2009; Ritz et al., 2010; Mouritsen and Hore, 2012).
After the suggestion of Klaus Schulten (Schulten et al.,
1978), it was shown that the compass orientation behav-
ior of night-migrating songbirds is influenced by the color
(i.e., wavelengths) of the light available in the room where
the orientation tests are performed (Wiltschko et al., 1993,
2010b). This wavelength dependence is difficult to explain
if the eyes and/or pineal organ are not somehow involved
in the magnetic compass. In birds, the pineal organ is not
needed for magnetic compass orientation (Schneider et al.,
1994), but photoreceptor molecules in the pineal organ
seem to be essential for magnetic compass orientation in
newts (Phillips et al., 2001).
It has been reported that oscillating magnetic fields at
specific resonance frequencies in the low-megahertz range
disrupt the magnetic compass orientation capabilities of
night-migratory songbirds (Ritz et al., 2004, 2009). A
recent double-blinded set of experiments has indicated that
the disruptive effects of low-megahertz range electromag-
netic fields are real, but that they are not limited to specific
resonance frequencies (Engels et al., 2014). Furthermore,
Engels et al. (2014) could show that anthropogenic electro-
magnetic noise, omnipresent in most urban environments
where birds and humans live, disrupts magnetic compass
orientation in migratory European Robins. The intensities
of the disruptive fields are ca. 1000 times lower than the
current WHO guideline limits for human exposure (Engels
et al., 2014). Such effects are still difficult to understand from
a theoretical perspective, but they are likely to be diagnostic
for the involvement of a fundamentally quantum mechani-
cal mechanism in the birds’ magnetic compass sense (Ritz
et al., 2009; Mouritsen & Hore, 2012; Engels et al., 2014).
On the molecular level, it has been shown that putatively
magnetosensitive cryptochrome molecules exist in the retina
of many vertebrates including migratory birds (Mouritsen
et al., 2004a; Möller et al., 2004; Liedvogel and Mouritsen,
2010; Niessner et al., 2011). Furthermore, cryptochromes
from migratory Garden Warblers (Sylvia borin) have been
shown to form long-lived radical pairs upon light excitation
(Liedvogel et al., 2007a), and effects of Earth-strength mag-
netic fields on a radical pair reaction in an artificially pro-
duced molecule mimicking the reaction principle thought to
take place in cryptochromes have supported the theoretical
feasibility of the suggested mechanism (Maeda et al., 2008;
reviewed in Mouritsen and Hore, 2012).
On the neuroanatomical level, a region named Cluster
N (Figure 8.11) is by far the most active forebrain region
when night-migrating birds perform magnetic compass
orientation, and this activation disappears when the birds’
eyes are covered (Mouritsen et al., 2005; Feenders et al.,
2008; Zapka et al., 2010). Cluster N consists of parts of
the hyperpallium and the dorsal mesopallium (Jarvis et al.,
2013) and is the lateral-most part of the visual Wulst in
European robins because Cluster N receives its neuronal
input from the eyes via the thalamofugal visual pathway
(Heyers et al., 2007). The presence and activation of Clus-
ter N at night has been independently replicated in another
night-migratory songbird, the Black-Headed Bunting
(Emberiza melanocephala) (Rastogi et al., 2011). Could
Cluster N be a processing center of light-dependent mag-
netic compass information?
Double-blind experiments with European robins have
shown that birds with bilateral Cluster N lesions were
unable to orient using their magnetic compass (Zapka et al.,
2009, see Figure 8.12). In contrast, sham Cluster N lesions
or bilateral sections of the ophthalmic branch of the trigemi-
nal nerves did not influence the robins’ ability to use their
magnetic compass for orientation (Zapka et al., 2009, see
Figure 8.12). Cluster N lesions only affect the magnetic
compass because Cluster N lesioned robins orient well
using their Sun and star compasses (Zapka et al., 2009, see
Figure 8.12). These data (1) show that Cluster N is required
for magnetic compass orientation in this species, (2) indi-
cate that Cluster N may be specifically involved in process-
ing magnetic compass information, (3) strongly suggest
that a vision-mediated mechanism underlies the magnetic
compass in this migratory songbird, (4) indicate that input
from the lagena is not sufficient for magnetic compass ori-
entation in robins, and (5) show that the proposed magnetic
input to the brain transmitted via the trigeminal nerve is nei-
ther necessary nor sufficient for magnetic compass orienta-
tion of European robins tested in an orientation cage (Zapka
et al., 2009; Mouritsen, 2013). The exact role of Cluster N
within the magnetic compass information processing cir-
cuit has not been determined, but the existing results raise
the distinct possibility that this small part of the visual sys-
tem enables birds to “see” magnetic compass information
(Mouritsen, 2013).
Do these results exclude the possibility that iron-
mineral-based and/or trigeminally mediated and/or lagena-
mediated magnetoreception exists? Absolutely not! In
birds, iron-mineral-based magnetoreception may very
well exist, and magnetic field-dependent neuronal activa-
tion in trigemino-recipient and lagena-recipient regions
has been documented (see previous section). Trigeminally
and lagena-mediated magnetoreception just does not seem
to be the primary mechanism for the magnetic compass
of night-migratory songbirds (Zapka et al., 2009), but it
could be a primary source for magnetic positional infor-
mation (Mora et al., 2004; Kishkinev et al., 2013). In fact,
it is likely that light-mediated, radical pair-based mag-
netoreception and iron-mineral-based magnetoreception

PART | II Sensory Biology and Nervous System Theme
128
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The trigeminal nerve is neither necessary nor sufficient for magnetic compass orientation in European robins. (A) The European robin (Photo ©
Henrik Mouritsen). (B–D) Bilateral sectioning of the ophthalmic branch of the trigeminal nerve (B) does not affect the birds’ magnetic compass orientation
capabilities (C, D; mN = magnetic North). (E–H) Bilateral chemical lesions of Cluster N (E) destroyed the magnetic compass capabilities of the birds (G),
whereas star compass orientation in a planetarium (F) and Sun compass orientation outdoors with view of the setting Sun (H) was unaffected by Cluster N
lesions. The circular diagrams are explained in the legend of Figure 8.3. (E) A schematic drawing and an example part of a brain section saggitally cut through
the center of Cluster N and stained with a neuronal marker. Scale bar = 500 μm. Rostral is left, caudal is right. Note that the tissue where Cluster N should
have been in the lesioned bird (E) is destroyed. Anatomy: A = arcopallium, E = entopallium, H = hyperpallium, ICo = intercollicular complex, M = mesopallium,
MD = mesopallium dorsale, MV = mesopallium ventrale, N = nidopallium, OT = optic tectum, P = pallidum. From Mouritsen (2013) after Zapka et al. (2009).
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FIGURE 8.11 Cluster N. (A) Cluster N is the most active brain area when migratory birds perform magnetic sensing and/or compass orientation at
night, and Cluster N is required for magnetic compass orientation (see Figure 8.12). (B) Cluster N is a part of the visual Wulst and receives input from
the eyes via the thalamofugal visual pathway (Heyers et al., 2007). Top view of the brain in gray indicates the medial-lateral and the frontal-caudal extent
of Cluster N and the DNH and DNH-shell. (C) Cluster N is a functional unit consisting of a part of the hyperpallium, a part of the dorsal mesopallium
(Jarvis et al., 2013), and a nucleus embedded within the hyperpallium and named DNH with a shell of cells around the DNH. Anatomy: A = arcopallium,
P = pallidum, E = entopallium, St = striatum, N = nidopallium, M = mesopallium, MD = mesopallium dorsale, MV = mesopallium ventrale, H = hyperpal-
lium, v = ventricle, OT = optic tectum, HF = hippocampal formation, IHA = HI = interstitial region of the hyperpallium intercalatum, DNH = dorsal nucleus
of the hyperpallium, DNH-shell = shell around the DNH, W = visual Wulst, LGd = Lateral geniculate nucleus, dorsal part, Rt = nucleus rotundus. Scale
bar = 0.5 mm. From Mouritsen (2013) after Mouritsen et al. (2005).

129Chapter | 8 Magnetoreception in Birds and Its Use for Long-Distance Migration
mechanisms exist side by side in several animal species
and that they may provide the animals with different types
of magnetic information (Wiltschko and Wiltschko, 2007;
Mouritsen and Hore, 2012).
As so often in biology, when there are two hypotheses
how something works, it often turns out that both of them are
correct to a certain degree. Furthermore, seemingly unnec-
essary redundancy seems to be a very common occurrence
in biology, probably because organisms that can perform a
function in several ways will be more robust to changes and
thus be favored by evolution (Mouritsen, 2013).
8.13 IRREPRODUCIBLE RESULTS AND
THE URGENT NEED FOR INDEPENDENT
REPLICATION
Magnetic sense research is strongly influenced by several
claims that nobody has ever been able to independently
replicate. This is particularly true for electrophysiological
evidence (Semm and Demaine, 1986; Beason and Semm,
1987), but there are also many other examples of contra-
dicting or irreproducible results in the literature, including
all claims that humans have a magnetic sense (Westby and
Partridge, 1986; Baker, 1989) and the claim that the mag-
netic compass of birds should only be located in their right
eye (Wiltschko et al., 2002, 2003; Liedvogel et al., 2007b;
Stapput et al., 2010; Hein et al., 2010, 2011; Engels et al.,
2012). These problems with reproducibility do not neces-
sarily mean that the original claims were wrong. However,
it means that any result in magnetoreception—and in any
other field for that matter—should be treated with caution
until a given finding has been independently replicated.
This lack of reproducibility in magnetic sense-related
research is unfortunately accompanied by an almost com-
plete lack of double-blind procedures. Considering its
history and the fact that humans have no intuitive feel for
magnetic stimuli (and therefore are less likely to detect even
obvious artifacts), double-blind procedures should become
the standard, and studies representing the first independent,
double-blind replication of key findings in magnetorecep-
tion are as important as the original finding (Mouritsen,
2013).
8.14 WHERE DO WE GO FROM HERE?
Although the magnetic senses are still not completely
understood, many studies from different fields support the
iron-mineral-based and the light-dependent magnetorecep-
tion hypotheses. However, fundamental questions remain in
all relevant fields.
For example, functional understanding of any particu-
lar iron-mineral-based structure proven to be involved in an
active sensory system is lacking (Mouritsen, 2012; Mourit-
sen and Hore, 2012). Likewise, we yet have to understand
biophysically how nature designed radical-pair receptors
so that they can be sensitive to Earth-strength magnetic
fields at physiological temperatures, a feat that has been
approximated, but not yet fully accomplished, in man-
made radical-pair reactions (Maeda et al., 2008; Rodgers
and Hore, 2009). Furthermore, studies at the protein level
suggest that bird cryptochromes have properties optimal for
magnetic sensing, such as formation of long-lived radical
pairs (Liedvogel et al., 2007a). However, we yet have to
demonstrate Earth-strength magnetic field effects on bird
cryptochromes at the protein level and in vivo.
On the neuroanatomical level, we have just begun to
explore the brain circuits processing magnetic informa-
tion, but we are still far from understanding how a bird gets
from the detection of magnetic information to a directional
choice, which is made based on integration of information
from multiple sensory systems. In addition, so far, none of
the reported responses of single neurons to magnetic stimuli
have been independently replicated. Even at the behavioral
level, where most studies about magnetic senses have been
published, a clear separation of experimental parameters
has proven difficult, and many behaviors appear to be mul-
timodal, or at least modulated by other modalities, such as
vision and olfaction (Mouritsen, 2013).
In conclusion, magnetoreception is an important part of
life for birds and a wide variety of other animals, and there
are still many opportunities to perform new, groundbreak-
ing research on the molecules, cells, and neural processes
underlying any kind of magnetoreception.
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