Magnetoreception in animals

Abstract

Like the theory of plate tectonics, the idea that animals can detect Earth's magnetic field has traveled the path from ridicule to well-established fact in little more than one generation. Dozens of experiments have now shown that diverse animal species, ranging from bees to salamanders to sea turtles to birds, have internal compasses. Some species use their compasses to navigate entire oceans, others to find better mud just a few inches away. Certain migratory species even appear to use the geographic variations in the strength and inclination of Earth's field to determine their position. But how animals sense magnetic fields remains a hotly contested topic. Whereas the physical basis of nearly all other senses has been determined, and a magnetoreception mechanism has been identified in bacteria, no one knows with certainty how any animal perceives magnetic fields. Finding this mechanism is thus the current grand challenge of sensory biology.

Full text

Like the theory of plate tectonics, the idea that ani-
mals can detect Earth’s magnetic field has traveled the path
from ridicule to well-established fact in little more than one
generation. Dozens of experiments have now shown that di-
verse animal species, ranging from bees to salamanders to sea
turtles to birds, have internal compasses. Some species use
their compasses to navigate entire oceans, others to find bet-
ter mud just a few inches away. Certain migratory species even
appear to use the geographic variations in the strength and in-
clination of Earth’s field to determine their position. But how
animals sense magnetic fields remains a hotly contested topic.
Whereas the physical basis of nearly all other senses has been
determined, and a magnetoreception mechanism has been
identified in bacteria, no one knows with certainty how any
animal perceives magnetic fields. Finding this mechanism is
thus the current grand challenge of sensory biology.
The problem is difficult for several reasons. First, hu-
mans do not appear to have the ability to sense magnetic
fields. Whereas most nonhuman senses, such as polarization
detection and UV vision, are relatively straightforward ex-
tensions of human abilities, magnetoreception is not. As a re-
sult, neither intuitive understanding nor the medical litera-
ture on human senses provides much guidance. Another
complicating factor is that biological tissue is essentially
transparent to magnetic fields, which means that magneto-
receptors, unlike most other sensory receptors, need not be
located on an animal’s surface and might instead be any-
where in the body. That consideration transforms a routine
two-dimensional visual inspection into a three-dimensional
search requiring advanced imaging techniques. Another im-
pediment is that large accessory structures for focusing and
otherwise manipulating the field—the analogs of eardrums
and lenses—are unlikely to exist because few materials of bi-
ological origin affect magnetic fields. Indeed, magnetorecep-
tion might be accomplished by a small number of micro-
scopic, possibly intracellular structures scattered throughout
the body, with no obvious structure devoted to magneto-
reception. Finally, the weakness of the interaction between
Earth’s field and the magnetic moments of electrons and
atoms, roughly one five-millionth of the thermal energy kT
at body temperature, makes it difficult to even suggest a fea-
sible mechanism.
The weakness of the field does provide one major ad-
vantage to researchers: It greatly limits the list of possible
physical detection mechanisms. Any suitable mechanism
would presumably have to involve a very sensitive detector,
amplification of magnetic interactions, or isolation from the
thermal bath. Interestingly, the three main mechanisms that
have so far been proposed—electromagnetic induction, ferri-
magnetism, and chemical reactions involving pairs of radi-
cals—are each based on one of those designs. The electro-
magnetic induction hypothesis, for example, is based on the
extremely sensitive electroreceptive abilities of some marine
species. The various hypotheses involving magnetite or other
ferrimagnetic materials are based on the powerful interaction
of such materials with magnetic fields. Finally, the radical-
pair mechanism relies on the relatively efficient isolation of
electron and nuclear spins from other degrees of freedom.
Different animals may detect magnetic fields in different
ways, and behavioral experiments and microscopic exami-
nations of possible magnetoreceptors have both yielded re-
sults that are consistent with all three mechanisms. Never-
theless, a magnetoreceptive organ has not yet been identified
with certainty in any animal. In this article we discuss the
physics of the three main mechanisms that have been pro-
posed and highlight some of the critical evidence in support
of each.
Electromagnetic induction
The Lorentz force causes a conducting rod moving through a
magnetic field to develop a nonuniform charge distribution. If
the rod is immersed in a conductive medium that is stationary
relative to the field, an electrical circuit is formed. As far back
as 1832, Michael Faraday noted that ocean currents should
generate electric fields as they move through Earth’s magnetic
field. Indeed, some modern profiling systems that detect and
map ocean currents are based on that principle.
Electroreception is relatively common and found in an-
imals ranging from aquarium fish to duck-billed platypuses.
Due to the weakness of Earth’s magnetic field, however, the
electromotive force induced in an animal moving at a realis-
tic speed can be detected only by a highly sensitive electro-
receptive system. In 1974, Adrianus Kalmijn suggested that
sharks and their close cousins, rays, possess such a system.
Those fish, collectively known as elasmobranchs, possess
several hundred long canals that begin at tiny pores in the
skin and end blindly inside the body (figure 1a). The canals,
which feature exceptionally resistive walls and an interior
filled with a highly conductive “jelly,” essentially function as
electrical cables. At the ends of the canals are the ampullae of
©
2008 American Institute of Physics, S-0031-9228-0803-010-X March 2008 Physics Today 29
Magnetoreception
in animals
Sönke Johnsen and Kenneth J. Lohmann
Determining how animals orient themselves using Earth’s magnetic field can
be even more difficult than finding a needle in a haystack. It is like finding
a needle in a stack of needles.
Sönke Johnsen is an associate professor of biology at Duke University in Durham, North Carolina. Ken Lohmann is a professor of
biology at the University of North Carolina at Chapel Hill.

Lorenzini—collections of cells that are extremely sensitive to
small changes in voltage. Because the canals are highly con-
ductive, almost all the induced voltage drop occurs at the
ampullae (figure 1b). The ampullae’s exact detection thresh-
old has been debated, but a conservative estimate is 2 μV/m,
the field that would be produced by a 1.5-V battery with one
electrode in New York Harbor and the other off Cape
Hatteras, North Carolina, 750 km south! Given that extraor-
dinary sensitivity, magnetoreception using induction is the-
oretically possible. Depending on its compass direction,
a shark or ray moving horizontally through the ocean at
1 m/s (about 2 miles per hour) could generate a voltage
gradient at the receptor as high as 25 μV/m, well above the
detection threshold.
In the several decades since the hypothesis was first pro-
posed, however, several findings have emerged that compli-
cate matters. First, although they
are exquisitely sensitive to
changes in voltage, the electro-
receptors of elasmobranchs were
found to be incapable of detect-
ing DC voltages. In addition,
ocean currents are also conduc-
tors moving through Earth’s
magnetic field and thus create
electric fields of their own.
Michael Paulin addressed both
problems in 1995 by suggesting
that sharks and rays might pay
attention only to the oscillating
electric fields that arise as their
heads sway rhythmically back
and forth during swimming. In
addition to creating AC voltages
that the animals can detect, the
head motion might function as a
high-pass filter, removing irrele-
vant stimuli associated with
ocean currents.
As one might guess, sharks
(and even rays) are not ideal ex-
perimental animals, and the evi-
dence for their magnetic sense is
not as complete as for that in
many other species. The few ex-
periments that have been done
mostly involved training captive
animals to respond to the pres-
ence of local magnetic field gra-
dients generated by an electro-
magnet. Given their extremely
sensitive electroreception, how-
ever, it is unclear whether the an-
imals responded to the magnetic
field or to the electric fields in-
duced as the magnet was turned
on and off. In addition, it has
never been demonstrated that
electromagnetic induction is re-
sponsible for any of the observed
magnetic behavior. In a 2001 ex-
periment by Michael Walker, rays
lost their ability to detect mag-
netic field gradients when small
magnets (but not nonmagnetic
brass bars) were inserted into
their nasal cavities. Since a mag-
net that moves with the detector should not affect an induc-
tion-based system, Walker and his colleagues interpreted the
results to mean that induction was not involved. But because
the bodies of rays are flexible, the possibility remains that the
magnets moved slightly relative to the electroreceptors and
thus affected an induction-based system.
It is also possible that freshwater and terrestrial animals
have induction-based mechanisms based on internal con-
ducting rods or loops such as neural circuits. However,
electromagnetic induction appears unlikely to be a wide-
spread mechanism for magnetoreception because only elas-
mobranchs are known to have the extreme electrical sensi-
tivity required. Most animals with electroreceptors have
electric thresholds two to five orders of magnitude higher—
too high for magnetoreception. For example, the electric fish
Eigenmannia (glass knifefish), a relatively electrosensitive
a
Pore 2
Pore 1
Ampulla 2
Ampulla 1
~0
~0
Dorsal
Ventral
vB×
h
vB×
h
vB×
h
B
h
v
ρJ
Voltage
b
−
+
Figure 1. Inductive magnetoreception. (a) Side view of a shark’s head, showing the
ampullae of Lorenzini electroreceptors (red dots) and jelly-filled conductive canals
(gray lines). The red lines are so-called lateral lines, used to detect vibrations in the
surrounding water. (Image courtesy of Chris Huh.) (b) Schematic showing two am-
pullae with their canals. As the shark swims east and into the page with a velocity v,
its movement across the horizontal component of Earth’s field, B
h
, causes a vertical
electromotive force of magnitude vB
h
. Because the shark’s body and especially its
skin are highly resistive, the voltage drop due to the current density ρJ results in no
potential difference between the dorsal and ventral surfaces of the animal. The high
conductivity of the canals, however, results in a large voltage drop across the ampul-
lae. The thick black lines illustrate the electric field surrounding and permeating the
shark. (Adapted from A. Kalmijn, IEEE Trans. Magn. 17, 1113, 1981.)
30 March 2008 Physics Today www.physicstoday.org

animal, would need to swim at 400 mph (nearly 180 m/s) to
detect Earth’s field using induction.
Ferrimagnetism
The only conclusively demonstrated magnetoreceptors are
found in various phytoplankton and bacteria, which contain
chains of crystals of ferrimagnetic minerals, either magnetite
(Fe
3
O
4
) or greigite (Fe
3
S
4
), as shown in figure 2 and on the
cover. The torque on the chain is so large that it rotates the
entire organism to align with Earth’s field. The field gener-
ally has a vertical component, and some of those organisms
use magnetoreception to sense what direction is “down” and
to move toward the deeper, less oxygenated mud they pre-
fer. The 1963 discovery by Salvatore Bellini of magnetotaxis
in certain bacteria, followed by Richard Blakemore’s 1975 de-
scription of the crystals, led to the detection of magnetite in
a diverse array of magnetoreceptive species, including
honeybees, birds, salmon, and sea turtles.
Ferromagnetic and ferrimagnetic minerals are natural
choices for a compass mechanism, due to their powerful in-
teraction with magnetic fields caused by spontaneous order-
ing of electron spins. Certain compounds of ferromagnetic el-
ements, including magnetite, maghemite (Fe
2
O
3
), and
greigite, are ferrimagnetic, meaning that although neighbor-
ing spins are antiparallel, the material still has a net moment
because the moments in one direction are larger than those
in the other. In both ferro- and ferrimagnetic minerals, the
minimization of energy that comes from spin alignment is su-
perseded at larger distances by other contributions to the
total energy primarily magnetostatic energy. Thus larger vol-
umes of those minerals are broken up into clearly defined do-
mains on the order of 0.1–1 μm in diameter, each of which
has a powerful magnetic moment in the absence of an exter-
nal field. A single cuboidal domain 60 nm on a side has an
interaction with Earth’s field roughly equal to kT.
In the presence of moderately strong external fields, en-
ergetically favorable domains expand at the expense of
neighboring domains, and the material as a whole becomes
a magnet. Lacking a source for such fields, however, ani-
mals’ internal compass needles are limited to their minerals’
original domain size. Particles larger than the typical domain
will develop multiple domains with moments in different di-
rections (figure 3a). Particles smaller than a certain size
(about 30 nm for magnetite, depending on the aspect ratio)
have their moments randomized by thermal energy, even
though the local spins are still aligned. In the single-domain
range, the magnetic interaction μB, where μ is the magnetic
moment of the particle and B is Earth’s field strength, must
be about six times greater than kT; otherwise even a tethered
compass will be tumbled too much by thermal interactions
www.physicstoday.org March 2008 Physics Today 31
10
–1
10
–2
10
–3
10
–4
10
–6
10
–5
VOLUME ( m)μ
3
0.2 0.4 0.6 0.8 1.0
ASPECT RATIO (width/length)
γθ= 10, <cos > = 0.9
γθ= 1, <cos > = 0.3
γθ= 0.1, <cos > = 0.03
Multidomain
Superparamagnetic
Single domain
1
0.8
0.6
0.4
0.2
0
0 5 10 15 20
0.06
0.02
0
0.04
<cos >θ
d/dσγ
⊥
γμ=/BkT
ab
1mμ
Figure 3. Magnetite
properties. (a) The
behavior of mag-
netite crystals de-
pends on their vol-
ume and aspect
ratio. Large particles
separate into multiple
domains, while small
particles are super-
paramagnetic, their
moments tumbled by
thermal fluctuations.
In the yellow region,
crystals are single
domain. The dashed
blue lines show three
different values of the
ratio γ of the mag-
netic energy μB to the thermal energy kT, and the associated average cosine of the angle θ between Earth’s field and the
crystal as it is buffeted by thermal agitation. The average cosine is given by the Langevin function, 〈cos θ〉 = coth(γ)–1/γ.
The animal symbols indicate the geometric parameters of the crystals found within them. (b) Alignment of the crystal
(black) requires the magnetic coupling to be roughly six times the thermal energy. But its sensitivity to changes in the field
strength, as determined by the derivative with respect to γ of the standard deviation of the component perpendicular to
field (red), peaks for ratios near 2. (Adapted from J. L. Kirschvink, M. M. Walker, in J. L. Kirschvink et al., eds., Magnetite
Biomineralization and Magnetoreception in Organisms, Plenum Press, New York, 1985.)
Figure 2. Bacterial magnetoreceptors. Transmis-
sion electron micrograph of the bacterium Magne-
tospirillum magnetotacticum showing the chain of
magnetosomes inside the cell. The magnetite crys-
tal incorporated in each magnetosome is about 42
nm long. (Image courtesy of Dennis Bazylinski.)

to be reliable (figure 3b). Bacteria thus may have found the
best strategy: long chains of single-domain particles. How-
ever, the most sensitive measurements of magnetic field
strength are found when the ratio of μB to kT is about 2.
Exactly how the rotation of a single-domain particle cre-
ates an action potential in a neuron is not known, but the ex-
istence of diverse mechanical sensors in cells offers many
possibilities. One is that the particles strain or twist hair cells,
stretch receptors, or other mechanical receptors as they at-
tempt to align with the geomagnetic field. Another is that the
rotation of intracellular magnetite crystals might open ion
channels directly if cytoskeletal filaments connect the crys-
tals to the channels.
The small size and ferric nature of those putative com-
passes make them almost impossible to unambiguously lo-
cate in a body. They are below the resolution limit of light
microscopy and are dissolved by many common tissue
preservatives. In addition, iron is one of the most common
metals found in organs and accumulates in a number of de-
generative processes, including hemochromatosis, Parkin-
son’s disease, and blood coagulation. Iron is also widespread
in both outdoor and lab environments. Thus searching for a
magnetite-based compass is even worse than finding a needle
in a haystack—it is like finding a needle in a stack of needles.
Evidence for magnetite receptors
Numerous techniques, including superconducting quantum
interference device magnetometry, x-ray fluorescence, and
atomic force microscopy, have been used in efforts to local-
ize magnetite-based receptors. So far, the best evidence has
come from trout and homing pigeons. In trout, confocal and
atomic force microscopy have found single-domain mag-
netite crystals in cells near a nerve that responds to magnetic
stimuli. In pigeons, a complex array of magnetic minerals has
been found in a part of the beak coupled to a nerve that re-
sponds to magnetic field changes. Six clusters of such miner-
als have been found, three on each side of the beak (figure 4).
The apparent functional unit, found in the branches of nerve
cells, consists of a vesicle 3–5 μm in diameter that is coated
with a noncrystalline iron compound and surrounded by
about 10 to 15 1-μm-diameter spherical clusters, each con-
taining approximately 8 million 5-nm-diameter crystals of
magnetite that alternate with chains of about 10 plates, each
roughly 1 × 1 × 0.1 μm, of maghemite. The functional units
32 March 2008 Physics Today www.physicstoday.org
Frontal
Median
Caudal
0.5 cm
100 mμ 5mμ 2mμ
a
b
cde f
Dorsal
Ventral
Lateral
Medial
Frontal
Caudal
25 nm
Figure 4. Evidence for magnetite-based magnetoreception. (a) The homing pigeon Columba livia provides some of the
best evidence. (b) X-ray image of the upper beak of C. livia, showing the three pairs of iron-containing areas and the
prevailing orientations of their neurons. (c) Stained section of the dendritic region in one of the areas. Dark areas are
iron deposits. (d) Schematic of a single neuron, showing the centrally located, iron-coated vesicle (light blue) and the clus-
ters of magnetite crystals (dark blue) alternating with rows of maghemite plates (red). (e) Hypothesized concentration of
magnetic flux in a neuron and its effect on the position of one of the magnetite clusters. (f) Magnetite cluster pulling away
from a membrane, which bends and opens a mechanically stimulated ion channel. (Panel a courtesy of Andreas Trepte;
panels b–c adapted from G. Fleissner et al., Naturwissenchaften 94, 631, 2007; panels d–e adapted from G. Fleissner et
al., J. Ornithol. 148, 643, 2007; panel f adapted from I. Solov’yov, W. Greiner, Biophys. J. 93, 1493, 2007.)

are regularly spaced at roughly 100-μm intervals in each of
the six locations. Interestingly, the orientation of the units in
each of three pairs of magnetic regions is perpendicular to
the other two pairs, which suggests a triaxial system.
Gerta Fleissner, Gunther Fleissner, and their colleagues
have proposed that the three different elements of the func-
tional unit have different functions (figure 4d–f). The
maghemite platelets, which are large enough to have ap-
proximately four magnetic domains, are thought to act as soft
magnets that locally amplify Earth’s field in the same way
that a soft iron core increases the strength of an electromag-
net. The amplified field then interacts with the clusters of tiny
magnetite crystals. Those crystals are too small to have a sta-
ble magnetic moment at body temperature. An applied field
will align the moments to a degree that depends on the field’s
strength and the temperature, but it will not rotate the parti-
cles themselves like compass needles. Termed superpara-
magnetic, such small particles of ferrimagnetic minerals have
magnetic moments that are weak compared with those of sin-
gle-domain particles. Nevertheless, Earth’s field, concen-
trated by the platelets, may be able to move or deform a large
enough cluster of the particles. Calculations based on the
morphology of the system suggest that when aligned with
Earth’s field, the maghemite platelets increase the local field
strength 20-fold, producing a force of about 0.2 piconewtons
on the 2.6-picogram magnetite clusters. The resulting move-
ment of the clusters might then open membrane channels ei-
ther through direct physical connections or by deforming the
nerve cell membrane. The function of the coated vesicle is un-
certain, though iron storage and additional field concentra-
tion have been suggested.
Because finding magnetic minerals in tissue is hard and
proving that they function in magnetoreception is harder,
some researchers have tested the hypothesis indirectly using
strong pulsed magnetic fields (about 500 μT for 5 ms) to alter
the direction of magnetization in single-domain magnetite
particles. After the pulses were applied, the magnetic orien-
tation of certain birds and sea turtles either vanished or was
slightly altered. However, given the high strength of the field
and the even larger induced electric field, it is impossible to
rule out effects on other compass mechanisms or even gen-
eral physiology.
Radical pairs
The third proposed magnetoreception mechanism involves
biochemical reactions. Although magnetic-field-dependent
chemical reactions are known, a magnetoreception system
based on chemistry must clear some high hurdles. First, in
Earth’s 50 μT field, energy shifts of molecular states due to Zee-
man splitting are only one five-millionth of kT at body tem-
perature (10
–27
versus 5 × 10
–21
joules); thus product yields and
rates of most chemical reactions will not be sensitive to weak
magnetic fields. But a class of chemical reactions involving
pairs of radicals shows an unusual sensitivity to the strength
and orientation of magnetic fields. For example, the rates of
certain redox reactions involving horseradish peroxidase are
slightly increased in fields of 1 mT. However, no room-
temperature reaction of any kind has shown a measurable ef-
fect at geomagnetic field strengths. Second, any such reaction
used for a compass requires immobilization of at least one of
the reactants, so that a constant orientation relative to the field
is maintained. With the exception of structural components,
biological molecules continually rotate and move. Even pro-
teins bound in cell membranes are in constant motion.
Assuming that spins are relatively isolated from ther-
mal effects, researchers interested in the possibility of chem-
ically mediated magnetoreception have focused on the cor-
related spin states of paired radical ions. The reaction, first
proposed by Klaus Schulten in 1982 and then developed by
Thorsten Ritz, begins with an electron transfer between two
molecules, leaving two unpaired electrons in a pure singlet
state. Over what is assumed to be a relatively long period
(about 100 ns), the spins interact with the nuclear spins and
precess at different rates that depend on the local magnetic
neighborhood and the orientation and strength of the geo-
magnetic field. Back-transfer of the electron can only occur
if the spins are oppositely aligned, and their alignment de-
pends on the length of the reaction and the difference in pre-
cession rates. Because the geomagnetic field can influence
the precession rate, it may be able, under the right set of
www.physicstoday.org March 2008 Physics Today 33
Figure 5. Cryptochrome is a candidate magnetoreceptor based on pairs of radicals. (a) The key components, illustrated
on this electron density image, are the chromophore flavin adenine dinucleotide and three tryptophan residues involved
with the chromophore’s reduction to the hydrogenated FADH. (b) Following cryptochrome excitation by a blue photon,
holes transfer from FADH through the chain of tryptophan residues (the reaction steps are labeled by their time con-
stants, and the tryptophans by their radical-state lifetimes). The resulting unpaired electron spins S
1
and S
2
precess
about the local magnetic field produced by the addition of the external magnetic field B and the contributions I
1
and I
2
from the nuclear spins on the two radicals. Hole back-transfer from tryptophan-324 to FADH quenches cryptochrome’s
active state but can occur only when the radicals’ electron spins are in a singlet state. (Adapted from I. A. Solov’yov,
D. E. Chandler, K. Schulten, Biophys. J. 92, 2711, 2007.)

conditions, to influence reaction rates or products.
In quantum mechanical terms, the initial singlet state is
coupled to a nearly degenerate triplet state via the hyperfine
interactions between the electron spins and the nuclear spins,
the coupling strength depends on the magnetic field, and the
rate at which the state acquires triplet character is thus field de-
pendent. If one assumes that the radical pair in the triplet state
forms a chemical product that differs from that of singlet pairs,
one has a potentially viable detector for weak magnetic fields.
It’s important to note that the radical-pair mechanism can de-
tect only the field’s axis, not its polarity. However, few animals
appear to be able to detect the polarity of Earth’s magnetic field
(exceptions are lobsters, salamanders, and mole rats). Instead,
they define “poleward” as the direction along Earth’s surface
in which the angle formed between the magnetic-field vector
and the gravity vector is smallest.
Because the influence of the geomagnetic field on sin-
glet-to-triplet conversion is very weak, the lifetime of the sin-
glet state due to other decay modes—such as fluorescence,
decoherence of the quantum state, and intramolecular con-
version—must be quite long for any appreciable magnetic ef-
fects to develop. Quantum mechanical calculations of model
systems, using plausible parameters, have shown that the
conditions can be met. In addition, the relationship between
the reaction time and the internal magnetic interactions must
be precise, and the molecules must contain few hydrogen or
nitrogen atoms, whose relatively strong magnetic moments
will overwhelm any effects due to Earth’s field. Furthermore,
the formation of the initial state must not randomize the spin
relationship of the two unpaired electrons. In general, that re-
quirement is met only in reactions begun by photoexcitation.
The cryptochrome hypothesis
The connection with photoexcitation has led to interest in a
group of blue-sensitive photoreceptive proteins known as
cryptochromes (figure 5a). Those molecules, which are quite
different from the usual proteins involved in vision, are often
involved in timing and biological rhythms in plants and an-
imals and were recently shown to cue the mass coral spawn-
ings on the Great Barrier Reef. They are attractive candidates
for magnetoreceptors because they are found in the eyes of
magnetoreceptive birds during migration and have a chro-
mophore that forms radical pairs after photoexcitation. In the
proposed reaction, an electron is donated to the chromo-
phore FAD (flavin adenine dinucleotide) from one of the
tryptophan amino acids in the protein (figure 5b).
Surprisingly, the best evidence that cryptochromes func-
tion in magnetoreception has come from plants. Intrigued by
persistent but controversial reports of weak magnetic fields
affecting plant growth, a group of researchers led by Mar-
garet Ahmad studied the growth of the small mustard plant
Arabidopsis thaliana, the botanists’equivalent of the laboratory
rat. Plants raised in a magnetic field of 500 μT grew much
more slowly than did control plants raised in the 50-μT geo-
magnetic field, but the inhibitory effect of the field occurred
only when the plants were raised under blue light (the color
that cryptochromes detect). Similar experiments in darkness,
in red light, and with mutant plants that had no cryp-
tochrome gene showed no growth inhibition in either field.
The finding demonstrated that cryptochrome mediates a
field-affected process, though not necessarily that cryp-
tochrome itself mediates the magnetic effect.
The photoexcitation possibility has inspired a large
number of experiments—mostly performed by Wolfgang
Wiltschko, Roswitha Wiltschko, and John Phillips—that have
examined animals’ magnetic orientation behavior under dif-
ferent wavelengths of light, on the assumption that the can-
didate molecules are in the visual system. The orientation be-
havior of many species has been found to change under spe-
cific wavelengths and intensities, but the results have been
bewildering, with different intensities and wavelengths of
lights leading to orientation in the correct direction in Earth’s
field, to random movements, or to orientation in the wrong
direction. The data are difficult to interpret, since they do not
fit the absorption spectra of any known photoreceptive mol-
ecule. An examination of the experiments on birds reached
only two general conclusions: Magnetic orientation is dis-
rupted when animals are exposed to light levels above 10
12
photons/(s·cm
2
) or to light at wavelengths greater than 565
nm (figure 6). Because dimmer, blue light occurs after sun-
set, the time when the birds begin to migrate, it is possible
that the ambient light simply signals the birds that it is time
to begin orienting in the appropriate migratory direction
rather than affecting any compass mechanism (twilight has a
visible irradiance less than 10
12
photons/(s·cm
2
) and is, of
course, blue). However, the pattern of responses is also con-
sistent with the cryptochrome hypothesis because long-
wavelength light temporarily deactivates the molecule.
A frequency of 1.315 MHz matches the electron spin res-
onance in the geomagnetic field. Hence, RF fields of that fre-
quency should interfere with the radical-pair mechanism. In
2005 Peter Thalau and his colleagues found that an oscillat-
ing magnetic field of that frequency, with an intensity of
0.48 μT, disrupted the orientation of the European robin. That
followed work by Ritz that showed that a 7-MHz field
(0.47 μT) and RF noise (0.085 μT at 0.1–10 MHz) both dis-
rupted orientation in the same animal. But in each case, the
effect might be attributable to the induced electric field. Both
Ritz and Thalau found that the RF fields did not disrupt mag-
netic orientation when the oscillating field was parallel to the
34 March 2008 Physics Today www.physicstoday.org
10
13
10
12
10
11
350 400 450 500 550 600 650 700
WAVELENGTH (nm)
IRRADIANCE (photons s cm )
−−12
Correct orientation
Disorientation
Figure 6. Photoexcitation experiments have explored
a possible connection between photoreceptors and
magnetoreception. The 40 different magnetoreception ex-
periments plotted here exposed three different migratory
birds (28 used the European robin, Erithacus rubecula;
9 the silvereye, Zosterops lateralis; and 3 the garden war-
bler, Sylvia borin) to single-wavelength LEDs. The error
bars denote the light’s full width at half maximum. Mag-
netic orientation was inhibited (blue points) by high inten-
sity or long-wavelength light. (Adapted from S. Johnsen
et al., J. Exp. Biol. 210, 3171, 2007.)

geomagnetic field, which appears to be a good control for
nonspecific effects. One caveat, however, is that RF experi-
ments on known radical-pair reactions found effects re-
gardless of how the RF field was aligned relative to the
ambient field.
Where next?
Biological systems often make ingenious use of physical prin-
ciples, and magnetoreception appears to be no exception. All
three proposed mechanisms can, in principle, get useful in-
formation from the weak geomagnetic field. However, with
the exception of magnetotactic bacteria, no mechanism has
been conclusively established.
Electromagnetic induction is based on straightforward
principles and appears to be within the capabilities of
sharks and rays, but its use has not been directly demon-
strated. The hypotheses based on ferrimagnetic minerals
have the best morphological evidence and a solid theoreti-
cal background. The most recent work in homing pigeons
also appears to get past the concern that the magnetic min-
erals are just contaminants.
The radical-pair mechanism is fascinating but enigmatic.
The conditions for its success are extremely strict. However,
evolution has built some equally improbable chemical facto-
ries, including the photosynthesis reaction center, which can
split water molecules using visible light. The biggest hurdle
for the radical-pair mechanism is not theoretical but how to
find the actual molecules involved. Through no fault of the
investigators, the current evidence for the radical-pair hy-
pothesis is maddeningly circumstantial. Cryptochrome is
photosensitive, is found in migratory birds, and forms radi-
cal pairs, but it has no direct links to magnetoreception. The
RF data are certainly suggestive, but they will be more so if
future experiments reveal an action spectrum in which some,
but not all, frequencies have an effect. In theory, such speci-
ficity should exist.
Magnetoreception research began with behavioral stud-
ies on relatively large migratory animals, but those animals
may not be ideal for understanding the mechanism. It may
be better to continue the work with zebrafish or fruit flies,
two magnetoreceptive species that are also model systems for
studying cellular and molecular processes. Regardless of the
experimental system used, the solution to the long-standing
mystery of magnetoreception in animals will almost certainly
come from a fascinating interplay of biology and physics.
We thank Rainer Johnsen for a critical reading of earlier versions of
this manuscript and for helpful discussions. The research was sup-
ported in part by grants from the National Science Foundation (IOB-
0444674 to Johnsen; IOS-0718991 to Lohmann).
Further reading
왘 D. A. Bazylinski, R. B. Frankel, Nat. Rev. Microbiol. 2, 217
(2004).
왘 G. Fleissner et al., Naturwissenschaften 94, 631 (2007).
왘 S. Johnsen, K. J. Lohmann, Nat. Rev. Neurosci. 6, 703 (2005).
왘 J. L. Kirschvink, D. S. Jones, B. J. MacFadden, eds., Mag-
netite Biomineralization and Magnetoreception in Organisms: A
New Biomagnetism, Plenum Press, New York (1985).
왘 T. Ritz, S. Adem, K. Schulten, Biophys. J. 78, 707 (2000).
왘 T. Ritz et al., Nature 429, 177 (2004).
왘 C. R. Timmel, K. B. Henbest, Phil. Trans. R. Soc. A 362, 2573
(2004).
왘 M. M. Walker et al., Nature 390, 371 (1997).
왘 R. Wiltschko, W. Wiltschko, Magnetic Orientation in Ani-
mals, Springer, New York (1995). 䊏
March 2008 Physics Today 35
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