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Magnetic compass orientation of migratory birds in the presence of a 1.315

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DOI: 10.1007/s00114-004-0595-8 · Source: PubMed

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Naturwissenschaften (2005) 92:86–90
DOI 10.1007/s00114-004-0595-8
SHORT COMMUNICATION
Peter Thalau · Thorsten Ritz · Katrin Stapput ·
Roswitha Wiltschko · Wolfgang Wiltschko
Magnetic compass orientation of migratory birds
in the presence of a 1.315 MHz oscillating field
Received: 18 August 2004 / Accepted: 11 November 2004 / Published online: 22 December 2004

Springer-Verlag 2004
Abstract The radical pair model of magnetoreception
predicts that magnetic compass orientation can be dis-
rupted by high frequency magnetic fields in the Mega-
hertz range. European robins, Erithacus rubecula, were
tested under monochromatic 565 nm green light in
1.315 MHz fields of 0.48 mT during spring and autumn
migration, with 1.315 MHz being the frequency that
matches the energetic splitting induced by the local geo-
magnetic field. The birds’ responses depended on the
alignment of the oscillating field with respect to the static
geomagnetic field: when the 1.315 MHz field was aligned
parallel with the field lines, birds significantly preferred
northerly directions in spring and southerly directions in
autumn. These preferences reflect normal migratory ori-
entation, with the variance slightly increased compared to
control tests in the geomagnetic field alone or to tests in a
7.0 MHz field. However, in the 1.315 MHz field aligned
at a 24 angle to the field lines, the birds were disoriented
in both seasons, indicating that the high frequency field
interfered with magnetoreception. These finding are in
agreement with theoretical predictions and support the
assumption of a radical-pair mechanism underlying the
processes mediating magnetic compass information in
birds.
Introduction
A magnetic compass of migratory birds was first de-
scribed almost 40 years ago in European Robins,
Erithacus rubecula. Meanwhile, it has been demonstrated
P. Thalau · K. Stapput · R. Wiltschko ()) · W. Wiltschko
Zoologisches Institut,
J.W.Goethe-Universitt Frankfurt,
Siesmayerstr. 70, 60054 Frankfurt am Main, Germany
e-mail: wiltschko@zoology.uni-frankfurt.de
T. Ritz
Department of Physics and Astronomy,
University of California,
Irvine, CA, 92697-4575, USA
in a variety of avian species, and its functional mode has
been analyzed in some detail by behavioral studies (for
summary, see R. Wiltschko and Wiltschko 1995). How-
ever, the question of how birds obtain directional infor-
mation from the geomagnetic field remained unanswered,
and only now we have begun to understand the primary
processes involved in magnetoreception.
A model proposed by Schulten (1982) and detailed by
Ritz et al. (2000) suggests that certain chemical reactions
such as radical-pair processes are sensitive to the direction
of the ambient magnetic field and thus can provide the
basis for a compass sense. The model links molecular-
level calculations of radical-pair reaction rates and yields
with predictions on the orientation. Many characteristics
of the avian magnetic compass, such as its being an ‘in-
clination compass’, its complex dependence on magnetic
intensity and on the ambient light conditions (see W.
Wiltschko and Wiltschko 2002), are rationalized as direct
consequences of radical-pair reactions.
An important prediction of the model is that the avian
magnetic compass should be disrupted by oscillating
magnetic fields at resonance frequencies in the low radio
frequency range (Ritz et al. 2000, Henbest et al. 2004).
This is indeed the case, as we recently demonstrated: a
disruptive effect of a broad band and a 7.0 MHz field was
observed when these fields were aligned at an angle to the
geomagnetic field; when the 7.0 MHz field was parallel,
in contrast, the birds’ orientation remained unaffected
(Ritz et al. 2004). These findings are consistent with the
radical-pair model.
Behavioral studies, however, have raised a novel ca-
veat. Under certain light regimes, migratory birds were
found to show oriented responses that did not represent
normal migratory orientation, because they did not un-
dergo the seasonal reversal in direction between spring
and autumn (W. Wiltschko et al. 2000a, b, 2003, 2004).
These ‘fixed-direction’ responses, whose mechanisms are
not yet fully understood, raise the important question
whether a response observed in a novel test condition is
indeed normal migratory behavior.

In view of this, the finding that the radio frequency
field parallel to the vector of the static geomagnetic field
did not alter the orientation behavior (Ritz et al. 2004)
seemed to require further analysis. Here we report tests
with robins performed in spring as well as in autumn in an
oscillating magnetic field with the frequency of
1.315 MHz. This is a special frequency as it matches the
energetic splitting induced by the local geomagnetic field
and thus results in a maximum effect. The oscillating field
was added to the local field again in two alignments,
parallel and at a 24 angle to the geomagnetic vector.
Methods
As in the previous study, the test birds were European Robins,
small passerines that migrate at night. The 12 birds tested in spring
were caught in early September 2002 in the Botanical Garden near
the Zoological Institute in Frankfurt am Main (50080 N, 8400 E).
They were kept in an indoor room in individual cages under a
photoperiod that simulated the natural one until December, when it
was reduced to LD 8:16 h. In the beginning of January 2003, the
photoperiod was increased to LD 13:11 h. This induced premature
Zugunruhe, and the spring experiments took place between 13
January and 17 February 2003. The 16 birds tested in autumn were
caught in early September 2003; they were kept under a photope-
riod simulating the natural one. We allowed about 2 weeks for the
birds to adjust to being in captivity; the autumn tests took place
between 22 September and 31 October 2003.
Testing followed standard procedures (for details, see Wiltschko
et al. 2001; Ritz et al. 2004). All tests took place in wooden huts in
the garden of the Zoological Institute, starting about the time when
the light went off in the housing cages and lasting for about 75 min.
The birds’ activity was recorded in funnel-shaped test cages made
from PVC. The inclined walls of the cages were lined with coated
paper (BIC, Germany, formerly TippEx) where the birds left
scratches as they moved. Each cage was placed in a cylinder made
from PVC and illuminated from above by monochromatic green
light with a peak wavelength of 565 nm and an intensity of 2.1 mW/
m2 within the test cage.
The oscillating fields of 1.315 MHz were produced as the fields
in previous tests (Ritz et al. 2004): we used coil antennas (2.1 m
diameter) consisting of a single winding of coaxial cable with 2 cm
of the screening removed. Each antenna was mounted on a wooden
frame surrounding four test cages and fed by amplified oscillating
currents from a high frequency generator (see Ritz et al. 2004 for
details). The 1.315 MHz fields had an average intensity of 485 nT,
i.e., about 1/100 of the intensity of the local geomagnetic field of
46,000 nT. Their intensity was measured before each test session
using a spectrum analyzer and a H-field probe; within the test
cages, the inhomogeneity was less than 15%, with variance be-
tween subsequent tests less than 20%.
The 1.315 MHz fields were added to the local geomagnetic field
(46,000 nT, 66 inclination) in two alignments, namely (1) parallel
to the field lines of the geomagnetic field and, for convenience, (2)
vertically, which means that there was an angle of 24 between the
axis of the oscillating field and the geomagnetic vector. Tests in the
local geomagnetic field alone served as controls.
The birds were tested in all conditions to obtain three evaluable
headings in each. Tests with less than 35 scratches were not in-
cluded in the analysis because of too little activity; as a result, some
birds have only two recordings in some conditions. From the
headings of the tests, we calculated a mean vector with direction ab
and length rb for each bird. The ab were comprised in grand mean
vectors with direction aN and length rN; they were tested for sig-
nificant directional preferences using the Rayleigh test (Batschelet
1981). The distribution of the mean headings in the various test
conditions and in spring and autumn were compared using the
Watson Williams test to look for differences in direction and, if
87
rN<0.6, the Mardia Watson Wheeler test to look for differences in
distribution (Batschelet 1981). The Mann Whitney U-test was ap-
plied to the angular differences of the ab values from the grand
mean aN in order to look for differences in variance.
Results
Table 1 gives the vectors of the individual birds; Fig. 1
shows the birds’ mean headings, together with the grand
mean vector, in the three test conditions in both seasons,
with the grand mean vectors given numerically in Table 2.
In the control tests in the geomagnetic field alone, the
robins significantly preferred their appropriate migratory
direction, north-northeast in spring and south-southwest
in autumn. With the 1.315 MHz field added to the geo-
magnetic field, the responses differed according to its
alignment with the geomagnetic field: when it was
aligned parallel to the magnetic vector, the birds contin-
ued to show a significant preference of their migratory
direction in spring as well as in autumn, with the seasonal
change in direction highly significant (p<0.001, Watson
Williams test). In both seasons, the grand mean vectors
point in the same directions as in the control tests in the
geomagnetic field (p>0.05, Watson Williams test), but
they are a little shorter, indicating an increase in scatter
(p<0.05, Mann Whitney U-test). However, with the os-
cillating field aligned vertically, i.e., at 24 to the geo-
magnetic field, the birds were no longer oriented. Their
behavior was significantly different from the corre-
sponding control tests (p<0.01 and p<0.001; Mardia
Watson Wheeler test), but there was no difference be-
tween seasons (p>0.05, Mardia Watson Wheeler test).
Discussion
The radical-pair model provides a diagnostic tool that
enables us to check whether or not a radical pair mech-
anism is involved in magnetoreception: application of
weak oscillating magnetic fields at distinct resonance
frequencies in the frequency range between 0.1 and
100 MHz should interfere with radical-pair reactions (Ritz
et al. 2000; Cintolesi et al. 2003; Henbest et al. 2004) and
thus disrupt the physiological processes leading to mag-
netoreception. The intensities required for the resonance
phenomena in question are so low that they would not
affect any of the other possible, magnetite-based mecha-
nisms of magnetoreception currently considered (e.g.,
Yorke 1979; Kirschvink and Gould 1981; Edmonds
1996). At the same time, the effect on the radical-pair
process is predicted to depend on the alignment of the
oscillating field with the static geomagnetic field (Can-
field et al. 1994; Henbest et al. 2004).
Our data are in agreement with this prediction: with
only 485 nT, the 1.315 MHz field was so weak that its
intensity was negligible compared to the 46,000 nT of the
geomagnetic field; hence its impact must be attributed to
a resonance effect. At the same time, it disrupted orien-
88
Table 1 Mean vectors of individual birds (n, number of tests per bird; ab, rb, direction and lengths of the mean vectors)
Bird Control: geomagnetic field 1.315 MHz, parallel to vector 1.315 MHz, 24 to vector
n ab rb n ab rb n ab rb
Spring 2003
02-1 3 26 0.98 3 19 0.31 3 170 0.72
02-2 3 20 0.76 3 313 0.66 3 313 0.55
02-3 3 47 0.91 3 30 0.39 3 336 0.99
02-4 3 350 0.72 3 171 0.15 3 20 0.86
02-5 3 15 0.94 3 20 0.99 3 306 0.94
02-6 3 1 0.94 3 64 0.28 3 140 0.42
02-7 3 18 1.00 3 57 0.97 3 33 0.17
02-8 3 20 0.99 3 318 0.53 3 117 0.48
02-9 3 354 0.97 3 356 0.94 3 226 0.50
02-10 3 24 0.82 3 338 0.77 3 220 0.94
02-11 3 358 0.81 3 87 0.82 3 60 0.32
02-12 3 37 0.79 3 15 0.95 3 16 0.24
Autumn 2003
03-1 2 207 0.95 4 154 0.44 2 260 0.97
03-2 3 251 0.36 3 140 0.98 2 100 0.80
03-3 3 178 0.89 3 218 0.84 3 147 0.37
03-4 3 204 0.65 3 223 0.98 3 208 0.73
03-5 3 166 0.91 2 198 0.95 2 225 0.70
03-6 3 176 0.99 3 180 0.96 3 270 0.41
03-7 3 197 0.83 3 112 0.46 3 278 0.34
03-8 3 204 0.87 3 235 0.55 3 227 0.31
03-9 3 207 0.90 2 326 0.15 3 274 0.32
03-10 3 194 0.77 3 153 0.99 3 67 0.98
03-11 3 218 0.99 3 204 0.88 3 69 0.47
03-12 4 181 0.74 3 199 0.89 3 164 0.82
03-13 3 174 0.20 3 226 0.84 3 330 0.34
03-14 3 176 0.95 3 203 1.00 2 99 0.84
03-15 3 193 0.74 3 173 0.62 2 348 0.80
03-16 3 134 0.49 3 309 0.23 3 355 0.32

Table 2 Grand mean vectors of the three test conditions in spring ences are given in parentheses. The last column indicates whether
and autumn (N, number of birds tested; aN, rN, direction and lengths the two distributions are significantly different by the Mardia
of the grand mean vectors, with asterisks indicating significance by Watson Wheeler test)
the Rayleigh test; non-significant directions or directional differ-

Test condition Spring Autumn Difference Significance

spring–autumn
N aN rN N aN rN
Control: 12 16 0.93*** 16 191 0.91*** 175 ***
geomagnetic field
1.315 MHz, 12 19 0.63** 16 197 0.65*** 178 ***
parallel to vector
n.s n.s
1.315 MHz, 12 (14) 0.15 16 (249) 0.14 (125) n.s
24 to vector
** p<0.01; *** p<0.001; n.s. not significant: p>0.05

tation only when aligned at an angle to the geomagnetic
field, but not when presented parallel. These results cor-
respond to those obtained in a 7.0 MHz field, where we
also observed disorientation only when that field was not
parallel to the magnetic vector (Ritz et al. 2004). This
suggests that the observed disorientation is indeed a direct
effect on the processes providing magnetic compass in-
formation, rather than a non-specific effect of radio-fre-
quency fields on motivation, etc. With the 1.315 MHz
field aligned parallel, the birds were oriented north-
northeast in spring and south-southwest in autumn—this
seasonal reversal of direction indicates that the directional
preferences must be considered normal migratory orien-
tation. Our present data thus clearly show that the
1.315 MHz field parallel to the geomagnetic field did not
disrupt the normal magnetoreception processes mediating
compass information, and it appears safe to assume that
this is also true for the 7.0 MHz field tested in the pre-
ceding study (Ritz et al. 2004).
The specific radio-frequencies affecting a radical-pair
process depend on the chemical composition and geo-
metrical structures of the molecules forming the radical
pair. At the present stage, it is not easy to predict exactly
which frequencies will interfere with the radical-pair
mechanism underlying magnetoreception, because the
nature of the molecules involved is not yet known. The-

Fig. 1 Orientation behavior of European robins during spring and
autumn under control conditions in the local geomagnetic field (C),
in an 1.315 MHz oscillating field aligned parallel to the field lines
of the geomagnetic field (1.3 MHz parallel) and in an 1.315 MHz
oscillating field aligned vertically, at a 24 angle to the field lines
(1.3 MHz 24). The triangles at the periphery of the circle indicate
the mean headings of individual birds; the arrows represent the
grand mean vectors proportional to the radius of the circle; the two
inner circles mark the 5% (dotted) and the 1% significance border
of the Rayleigh test (Batschelet 1981)
oretical and in vitro studies indicate that for typical bio-
molecules, resonances are expected within the 0.1–
100 MHz range. Furthermore, these resonances are in
general very broad and might therefore lead to disturbing
effects at virtually all frequencies in this range provided
that the intensity of the oscillating field is sufficiently
strong (Woodward et al. 2001, 2002; Henbest et al. 2004).
A special resonance occurs when the frequency of the
oscillating field matches the energetic splitting induced
by the static (geomagnetic) field, i.e., at 1.315 MHz for
the 46,000 nT local geomagnetic field in Frankfurt. Hence
one expects a marked effect of a 1.315 MHz oscillating
field, irrespective of the nature of the molecule involved.
We indeed observed disorientation when the
1.315 MHz field was aligned at a 24 angle. In the parallel
89
alignment, on the other hand, we obtained in both seasons
vectors that were shorter than those in the respective
control tests in the geomagnetic field. They reflect a
significant increase in variance. This may have trivial
reasons, as we cannot exclude that the field was occa-
sionally slightly off the intended alignment, despite of all
the care that was taken not to touch the coil antenna when
we had to slip in for placing the birds in the test cages etc.
On the other hand, when the 7.0 MHz field was aligned
parallel, the technical problems were similar, but the
birds’ orientation had been statistically indistinguishable
from that in the geomagnetic field alone (see Ritz et al.
2004). So the increased variance could be due to the more
pronounced effect expected at the 1.315 MHz resonance
compared to resonances at 7.0 MHz and other frequen-
cies. It appears possible that the 1.315 MHz field may
have a certain effect on magnetoreception also when it is
aligned parallel to the geomagnetic field, making it
slightly more difficult, but not impossible for birds to
obtain directional information from the geomagnetic
field.
Future theoretical studies will be needed to assess
whether the seemingly stronger effect of a 1.315 MHz
field is a consequence of the different nature of the res-
onance at 1.315 MHz, which is a resonance with the
splitting induced by the external static field as opposed to
the internal fields by magnetic nuclei at other frequencies.
In further experiments, it will be a challenging task to
identify additional frequencies that will affect the pro-
cesses leading to magnetoreception in a strong way. By
determining such an action spectrum, we may be able to
derive information on the structure of the molecules in the
radical-pair mechanism and eventually can hope to
identify the photopigments involved in the primary pro-
cesses of magnetoreception.
Acknowledgements Our work was supported by the Deutsche
Forschungsgemeinschaft (W.W.) and by the Fetzer Institute (T.R.).
We gratefully acknowledge the technical support of the T-Systems,
Germany, especially of H. Kpper, T. Loppnow and B. Marx, and
we thank F. Galera, S. Hilmer, C. Koschella and S. Mnzner for
their valuable help with bird keeping and conducting the experi-
ments
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