Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior
1 Fachbereich Biologie und Informatik, Zoologie, J. W.
Goethe-Universität Frankfurt am Main, Siesmayerstrasse 70, D 60054
Frankfurt am Main, Germany
2 Department of Environmental Sciences, University of Technology, Sydney, PO
Box 123, Broadway, NSW 2007, Australia
3 Division of Geological and Planetary Science, The California Institute of
Technology, Pasadena, CA 91125, USA
4 Department of Earth and Planetary Sciences, University of Tokyo, Hongo
Campus, Tokyo, Japan
* Author for correspondence (e-mail: wiltschko{at}zoology.uni-frankfurt.de)
Accepted 9 July 2002
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Summary |
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Key words: magnetoreception, single domain magnetite, superparamagnetic particles, pulse, biasing field, migratory orientation, Zosterops l. lateralis, Australian silvereye
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Introduction |
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Birds have always been of particular interest for the study of
magnetoreception because they rely strongly on the Earth's magnetic field for
orientation and navigation. They appear to use information from the
geomagnetic field in two ways, namely (1) as a compass for direction finding
and (2) as part of their navigational `map' for determining positions (for a
review, see R. Wiltschko and Wiltschko,
1995). These probably involve separate receptor systems with
different types of receptor cells, as the biophysical constraints on them
differ markedly (e.g. Kirschvink and
Walker, 1985
). In birds, magnetite was found in the head,
particularly in the ethmoid region above the beak
(Walcott et al., 1979
;
Beason and Nichols, 1984
;
Beason and Brennan, 1986
;
Kirschvink and Walker, 1986
;
Edwards et al., 1992
) and in
the cutis of the upper mandible (Hanzlik
et al., 2000
; Winklhofer et
al., 2001
). These parts of the head are innervated by the
ophthalmic nerve, a branch of the nervus trigeminus;
electrophysiological recordings from this nerve and from the trigeminal
ganglion of Bobolinks Dolichonyx oryzivorus (Icteridae) revealed
units that responded to changes in the intensity of the magnetic field (e.g.
Beason, 1989
;
Semm and Beason, 1990
).
Similar work in fish also confirmed the role of the ophthalmic nerve and led
to the ultrastructural identification of a cell containing single-domain
magnetite, which could serve as the much sought-after magnetoreceptor
(Walker et al., 1997
;
Diebel et al., 2000
). In view
of these findings, it seemed promising to look for a possible involvement of
magnetite-based receptors in the orientation processes of birds by behavioral
studies.
Since the magnetite particles found in birds appeared to be single domains
(Walcott et al., 1979;
Kirschvink and Walker, 1986
;
Beason and Brennan, 1986
;
Beason, 1989
;
Edwards et al., 1992
), the
easiest approach seemed to be to alter the magnetization of these particles
with a brief but strong magnetic pulse. If they were involved in receptive
processes, this could lead to a dramatic change in the information they
mediated, which, in turn, should cause a marked change in the birds'
orientation behavior. In studies performed by some of the authors (U.M., R.W.,
W.W.), treatment with a strong pulse had a considerable effect on the
migratory orientation of Australian silvereyes, Zosterops lateralis,
deflecting the birds' headings from their natural migratory direction by
approximately 90° towards the east for about 2 days (W. Wiltschko et al.,
1994
,
1998
). Similar behavioral
changes were observed in other passerine migrants (Beason et al.,
1995
,
1997
;
W. Wiltschko and Wiltschko,
1995
; Beason and Semm,
1996
). However, this effect was restricted to experienced birds
that had already completed at least one migration trip; naive birds tested
during their first migratory season remained unaffected and continued in their
migratory direction (Munro et al.,
1997a
,b
).
The latter finding suggested that the effect of the pulse must involve an
experience-dependent system and, together with the responses to changes in
intensity recorded from the ophthalmic nerve
(Beason, 1989
;
Semm and Beason, 1990
), led to
the conclusion that a possible magnetite-based receptor provides magnetic
`map' information by measuring intensity and is part of a system indicating
position (for discussion, see W. Wiltschko
and Wiltschko, 1998
). The experiments by Beason and Semm (1986)
also suggested that the pulse affected the `map', not the compass. In
displaced homing pigeons, the pulse effect was less pronounced and more
variable, which is attributed to the multi-factorial nature of the pigeons'
navigational `map' (Beason et al.,
1997
).
The experimental procedures applied in these experiments were criticized by one of us (J.K.) for reasons given below. So we decided to collaborate and perform the study described here, where we modified the experimental technique in order to obtain a more predictable effect on the magnetite particles involved in a possible receptor.
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Theoretical background of the experiments |
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Kalmijn and Blakemore
(1978) reported the first
pulse remagnetization experiments on the magnetotactic bacteria. To guarantee
that the magnetic pulse was aligned so that it was antiparallel to the
magnetic direction of the bacteria, they first used a static magnetic field
(approximately 1 mT; about 20 times stronger than the geomagnetic field) to
align the bacteria and then applied a brief pulse (approximately 1 µs).
Strong pulses antiparallel to the direction of this biasing field were able to
completely reverse the swimming direction of all bacteria present, indicating
that the magnetosomes had been remagnetized in the reversed direction, whereas
pulses parallel to the bias field had no effect
(Diaz-Ricci at al., 1991
).
In experiments with birds (Wiltschko et al.,
1994,
1998
; Beason et al.,
1995
,
1997
), the situation was
different. The only `biasing field' present before and during treatment was
the much weaker geomagnetic field. The birds were magnetized `south anterior',
as defined by Beason et al.
(1995
), while facing east, that
is, the pulse was applied perpendicular to that field. The very fact that the
pulse remagnetization experiments did have an effect on the birds' behavior
argues strongly that a magnetite-based receptor of some sort is involved, as
no other known biophysical mechanism for transducing the geomagnetic field to
the nervous system would show any effect after pulse treatment. However, the
observed 90° change in direction did not allow any conclusions about the
nature and specific arrangement of magnetite with the receptor system.
Mann et al. (1988 isolated
chains of single domain particles from the ethmoid region of sockeye salmon
Oncorhynchus nerka and, more recently, Walker et al.
(1997
) and Diebel et al.
(2000
) described chains of
single domains in the lamina propria layer within the olfactory
lamellae of the rainbow trout Oncorhynchus mykiss. As magnetic
measurements (e.g. Beason and Nichols,
1984
; Beason and Brennon, 1986;
Edwards et al., 1992
) had
indicated the presence of single domains also in the heads of birds (see also
Kirschvink and Walker, 1986
),
it seemed reasonable to assume that similar chains of single domain magnetite
are part of a possible magnetoreceptor. If such magnetosome chains were free
to move to some extent, a pulse perpendicular to a weak biasing field is
expected to remagnetize roughly half of the magnetosomes, and may actually
produce some heterogeneously magnetized chains, causing some of them to kink
or bend. The effect of the pulse on a possible receptor structure could thus
not be clearly defined. This was pointed out by one of us (J.K.), who
suggested that we use a procedure similar to that by Kalmijn and Blakemore
(1978
) on the magnetotactic
bacteria. The `bacteria-like' configuration is clearly the simplest hypothesis
for the construction of a magnetite-based receptor (e.g.
Kirschvink and Gould, 1981
)
and lends itself to similar tests via pulse-remagnetization: if the
magnetite particles in a receptor were single domains arranged in magnetosome
chains that were free to move, a strong biasing field could be used to rotate
and reliably align them in the direction of that field. Application of a pulse
antiparallel to that direction should remagnetize them all, thus producing a
maximum effect, whereas a pulse parallel to that direction would have little
or no effect. The present study was designed to test whether the above
prediction was correct.
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Materials and methods |
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Test birds
As in the previous studies, the test birds were Australian silvereyes of
the migratory Tasmanian population, Zosterops l. lateralis (Latham).
These birds migrate in flocks predominantly during the twilight hours at dawn
and dusk (Lane and Battam,
1971; Chan, 1995
);
they cross Bass Straight to spend their winter on the Australian
continent.
The test birds were captured in Hobart, Tasmania, between 1 and 3 February,
1998. They were aged according to scull ossification
(Pyle et al., 1987) and
plumage characteristics (A. Leishman, personal communication). Twenty adult
individuals were selected for the present study. The birds were transferred by
airplane to Sydney and housed in a laboratory building on the Kuring-gai
campus of the University of Technology, Sydney.
Test conditions and performance
All tests took place in a wooden hut at the Kuring-gai campus in the local
geomagnetic field (57 500 nT, -64° inclination). Testing followed a
standard sequence: it began with a series of six control tests to determine
the directional preference of each individual in order to assure that the
birds showed appropriate migratory behavior and to document the stability of
the directional choices from day to day. A single test performed immediately
after exposure to a biasing field was to check whether this field by itself
would affect behavior. Two critical tests after treatment with the pulse in
the presence of the biasing field completed the sequence, the first one
starting immediately after treatment, the second one taking place the
following day.
In view of these critical tests, the birds were subdivided into two groups, PAR and ANTI, according to the direction of the biasing field in relation to the direction of the pulse. One bird escaped during the initial phase; therefore, the group ANTI consisted of nine birds and group PAR of ten birds.
The biasing field was 1 mT, approximately 20 times the earth field's
intensity, produced by Helmholtz coils, with magnetic north in geographic east
for the ANTI-birds and in geographic west for the PAR-birds. It added to the
local geomagnetic field so that the north directions of the combined fields
deviated from east and west, respectively, by about 2° towards north. The
birds were exposed to the combined field for about 5 s while facing geographic
east, which meant magnetic north for the ANTI-birds and magnetic south for the
PAR-birds. The pulse, of intensity 0.5 T and duration approximately 4-5 ms,
was identical to the one used in earlier studies and was administered in the
same way (W. Wiltschko et al.,
1994,
1998
), being `south anterior'
as defined by Beason et al.
(1995
,
1997
). This pulse was applied
while the birds were exposed to the 1 mT biasing field oriented as before,
which means that the pulse was parallel to the field for the PAR-birds and
antiparallel for the ANTI-birds.
All the birds in each group were tested simultaneously every second day, except for the critical tests that took place on 2 consecutive days. Testing started approximately 30 min before the lights went off in the housing room and ended after approximately 75 min. The light level of the diffuse light in the test cages was about 5 lx.
Data recording and analysis
Orientation was recorded in funnel cages (see
Emlen and Emlen, 1966) lined
with typewriter correction paper (Bic, formerly Tipp-Ex, Germany). The birds
were tested one in each cage; they left scratches in the coating of the
inclined wall when they moved. For evaluation, the paper was removed, divided
into 24 sectors, and the number of scratches in each sector counted.
Recordings with fewer than 35 scratches were excluded because of insufficient
migratory activity.
From the distribution of activity, we calculated the heading of each
recording. To characterize the behavior during the control phase, we
calculated the individual birds' mean vectors from up to six control headings
per bird, and, on the basis of the mean headings, calculated grand mean
vectors for the two groups by vector addition. To assess the effect of the
treatment, mean vectors were calculated from the headings recorded (up to 10)
each testing day, which were tested using the Rayleigh test for directional
preference. The axial vector was obtained by doubling the angles and
retransformation (see Batschelet,
1981).
The behavior of the two groups was compared using the
MardiaWatsonWheeler test
(Batschelet, 1981) on the
original distribution and the distribution of the doubled angles. With the
same test, we also compared the behavior of the birds after exposure to the
bias field and pulse treatment with that during the control phase before
treatment.
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Results |
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The well oriented behavior of our test birds in their northerly migratory direction during the control phase is obvious. Most individual birds have long vectors (see Fig. 1A). The grand mean vectors based on the birds' mean headings, with 11°, 0.98 for the PAR-group and 2°, 0.87 for the ANTI-group, were both highly significant (P<0.001, Rayleigh test). The ANTI-group appears to show slightly more scatter; statistically, however, the two groups do not differ from each other before treatment (P>0.05; MardiaWatsonWheeler test). Exposure to the biasing field of 1 mT alone did not have a noticeable effect on the orientation behavior (Fig. 1B); the directional preferences did not differ from those in the control phase (P>0.05 for both groups and all six control days).
After treatment with the pulse in the presence of the biasing field, both groups changed their behavior (PAR: P<0.05, all control days except day 2; ANTI: P<0.05, all control days except day 6). The birds were no longer oriented in their migratory direction, but showed a significant preference for an axis that roughly coincided with the eastwest axis (Fig. 1C), which was more pronounced on the second day after treatment, with more headings in the westerly direction. Again, there was no difference between the PAR birds and the ANTI birds, both groups showing the same pattern (P>0.05; see Table 1). This means that the direction of the pulse with respect to the biasing field had no effect on the response.
It is impossible to decide whether the observed response represents a preference for the magnetic eastwest axis or a preference for an axis perpendicular to the migration axis. With the migratory direction being so close to north, the confidence intervals include both axes.
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Discussion |
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What type of magnetoreceptor is suggested by the response of the birds and,
respectively, what type of receptor is compatible with our results? One
possibility is that a magnetoreceptor contains single domains with limited
freedom of motion under normal conditions, so that some of them had not been
aligned in the biasing field and, as a consequence, were remagnetized in the
PAR situation. Magnetoreceptors, which have evolved to extract an intensity
signal from the geomagnetic field, do not necessarily need to have a full
range of motion (for a discussion, see
Kirschvink and Gould, 1981;
Kirschvink and Walker, 1985
).
A magnetic pulse, applied to magnetosomes that are not free to move, is likely
to produce chains that are heterogeneously magnetized. It is impossible to say
what the output of a receptor altered this way might mean to the birds; it
could result in behaviors similar to those reported from the previous studies
(W. Wiltschko et al., 1994
,
1998
) or observed in the
present one.
Another possibility, however, is that the idea of an avian intensity
receptor based on single domains arranged in chains might not be correct. One
aspect of the previous pulse experiments (Wiltschko et al.,
1994,
1998
) that has always been
hard to explain is the short duration of the effect. A clear effect was
observed only on the day of treatment itself and the day after treatment;
after a week of apparent disorientation, the migrants returned to their normal
migratory direction (W. Wiltschko et al.,
1994
,
1998
). Because remagnetization
of single domains should be as stable as the original one, it is difficult to
see how the previous state could be restored, and one must turn to auxiliary
assumptions. One possibility is that some as-yet-unknown mechanisms allow the
particles to gradually realign themselves in their original position during a
week's interval of time, thus `healing' and letting the birds recover their
normal behavior. Single domain particles magnetized in opposite directions to
the remainder of the chain would represent a high-energy state; hence it seems
possible that the odd magnetite crystals rotate back into alignment within the
receptor structure. This might lead to entire chains of particles magnetized
in the opposite way from their original magnetization, but if it is only the
magnitude of the magnetic moment of the particles, not their polarity, that
determines the output of the receptor (see
Kirschvink and Walker, 1985
),
this would not affect its functionality. By contrast, we cannot exclude the
possibility that the fading of the effect may reflect a purely behavioral
response. Although recalibration of a component of a position-locating system
appears hardly possible as long as the birds are restricted to the small space
of a cage (in contrast to pigeons that are released and home over considerable
distances; see Beason et al.,
1997
), they might realize a continuing discrepancy between the
input of a magnetite-based receptor and other cues involved in a
multifactorial `map'. This might cause them to simply ignore the information
from that receptor, falling back on their innate migratory direction.
Histological studies looking for magnetite particles in birds have not yet
produced clear evidence for single domains. Magnetosome chains, similar to
those described in bacteria, have been found in fish, another vertebrate group
(Mann et al., 1988;
Diebel et al., 2000
). In
birds, single domains were indicated mostly by magnetic property measurements
(Walcott et al., 1979
;
Beason and Nichols, 1984
;
Beason and Brennon, 1986; Edward et al., 1997); the isolated crystals of
magnetite that were imaged (Kirschvink and
Walker, 1986
) had been extracted from the head of pigeons without
any indication of their original position. Iron deposits in the tissue, in
part associated with fibers of the ophthalmic nerve, have been identified
using Prussian Blue (Beason and Nichols,
1984
; Williams and Wild,
2001
), but it has not been demonstrated whether they are in fact
magnetite. In short, single domain crystals as such have not yet been
demonstrated in their natural position embedded in the tissue as part of a
receptor in birds, yet the existence of the relatively small numbers of single
domains needed to explain the magnetoreceptive behavior cannot be excluded
either. Hanzlik et al. (2000
)
and Winklhofer et al. (2001
)
recently identified magnetite particles of the much smaller size of
superparamagnetic grains (SPM) in the skin of the upper beak of pigeons, that
is, in the region of the receptive fields of the ophthalmic nerve. They were
found within the subcutis, arranged in well defined clusters surrounded by a
sheath of neurofilaments.
Since superparamagnetic crystals do not have stable magnetic moments, their magnetization remains unaffected by the pulse; similarly, the pulse would cause hardly any physical torque or translations, so that significant displacements of the crystals or mechanical damages of the receptor structure appear to be rather unlikely. In view of this, it is difficult to see how the pulse could affect a receptor based on superparamagnetic particles to cause the observed effect. Nevertheless, a pulse of about 10,000 times the earth field intensity represents an extremely strong signal to any receptor detecting magnetic intensity. The nature of the structures transmitting the signals is still unknown; a temporary impairment of a receptor built to record minute intensity differences cannot be totally excluded.
Our behavioral study is thus able to exclude the hypothesis that freely
mobile chains of single domains are a component of the possible receptor, but
it does not allow us to decide between the other possibilities. Little is
known about the specific size of the magnetite particles in birds and in what
structure they are embedded. So far, more detailed studies are only available
for salmonid fish (Walker et al.,
1997; Diebel et al.,
2000
). Recent work by Williams and Wild
(2001
) clearly indicates that
the iron-containing structures in the beak of pigeons, although also
innervated by a branch of the nervus trigeminus, are different in
location and structure. Here, we must hope for new histological studies that
identify magnetite particles in situ in the tissue of birds and at
the same time show details of the receptor structure and connections to the
nervous system.
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Acknowledgments |
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