Light-dependent magnetoreception in birds: analysis of the behaviour under red light after pre-exposure to red light
Fachbereich Biologie und Informatik, Zoologie, J. W. Goethe-Universität Frankfurt, Siesmayerstrasse 70, D-60054 Frankfurt am Main, Germany
* Author for correspondence (e-mail: wiltschko{at}zoology.uni-frankfurt.de)
Accepted 13 January 2004
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Summary |
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Key words: migratory orientation, magnetoreception, magnetic compass, wavelength dependency, photopigment, Erithacus rubecula
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Introduction |
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Because the initial step of the proposed mechanism is photon absorption,
magnetoreception would be light dependent. Results of behavioural experiments
with homing pigeons and caged migratory birds support the model by indicating
that magnetoreception indeed occurs in the eye
(W. Wiltschko et al., 2002a)
and that light from a certain wavelength range is required for magnetic
compass orientation. Migratory birds were well oriented in their migratory
direction in the presence of light from the blue and green part of the
spectrum up to 565 nm, whereas they were disoriented under monochromatic 590
nm yellow or 635 nm red light (see W.
Wiltschko and Wiltschko, 2002
for a review). These experiments
used LEDs (light-emitting diodes) with a range of half bandwidths of
30
nm to produce the test light; a recent study using even narrower bandwidths of
10 nm produced by interference filters reported disorientation already at
568 nm (Muheim et al., 2002
).
The wavelength range of vision in birds extends up to
680 nm
(Maier, 1992
); the range
allowing magnetic compass orientation thus seemed to be markedly shorter, with
the long-wavelength part of the visual spectrum not being able to initiate the
processes leading to magnetoreception.
This seemed strange, because neurophysiological recordings from the nucleus
of the basal optic root (nBOR) in pigeons had identified direction-selective
cells that responded to magnetic stimuli under long-wavelength light. Some
cells showed peak responses at 580 nm and continued to respond at a fairly
high level up to 674 nm (Semm and Demaine,
1986), i.e. at wavelengths that appeared to be beyond the birds'
range for compass orientation. This discrepancy between electrophysiological
and behavioural data on the wavelength dependency of magnetoreception in birds
caused us to analyse further the behaviour under red light. If neurons
responding under red light carried information about the magnetic field, one
might expect that birds were, in principle, able to make use of this
information.
An earlier study had shown that exposing robins to magnetic intensities
outside the normal functional window of the magnetic compass enabled these
birds to orient at the respective intensities
(W. Wiltschko, 1978). By
analogy to these experiments, we pre-exposed European robins to red light
before testing them under the same red light, and when they were found to be
oriented (Möller et al.,
2001
) we began to analyse this orientation by varying the
pre-exposure conditions and comparing the response under red light to that
under green light.
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Materials and methods |
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Test birds
Our test birds were European robins (Erithacus rubecula,
Turdidae), small passerines that migrate at night. All birds were young ones
in their first year of life that had been mistnetted during autumn migration
in September and early October 1998, 1999 and 2000 in the Botanical Garden
near the Zoological Institute in Frankfurt a.M. (50°08' N,
8°40' E). They were housed indoors in individual cages under a
photoperiod that simulated the natural one, gradually decreasing from 13 h:11
h L:D in early September until 8 h:16 h L:D was reached in December. The
autumn tests in 2000 with 16 birds were carried out while the birds stayed
under this photoperiodic regime.
For the spring experiments, we increased the photoperiod after New Year to 13 h:11 h L:D in order to induce premature spring migratory activity so that the tests could start in the first half of January. After the tests were completed, the robins remained in captivity until the last week of March when the natural photoperiod outside had reached 13 h:11 h L:D; then they were released.
Test conditions
All tests took place in wooden houses in the garden of the Zoological
Institute in the local geomagnetic field (46 000 nT, 66° inclination). The
test lights were monochromatic red and green lights produced by LEDs. In 1999,
we used the same red LEDs as in previous studies (e.g.
Wiltschko et al., 1993;
W. Wiltschko and Wiltschko,
1995
), with a peak wavelength of 635 nm, with
/2 at 617 nm
and 657 nm. In 2000, another type of LED with a peak wavelength of 645 nm and
/2 at 625 nm and 666 nm was used. Tests in 1999 under both types of
red light had shown that the birds' behaviour did not differ in any way (see R
and R2 in Table 1,
upper section). The green LEDs were the same as those used in previous
experiments (e.g. W. Wiltschko and Wiltschko,
1995
,
1999
), with a peak wavelength
of 565 nm and
/2 at 553 nm and 583 nm. The intensity of the red and
green test light was adjusted to be at an equal quantal flux of
67x1015 quanta s1
m2 (test conditions R, G), an intensity where birds in
earlier tests had shown excellent orientation under green and blue light (see
W. Wiltschko and Wiltschko,
2002
). This corresponded to 2.0 mW m2 and 1.8 mW
m2 for red light and 2.4 mW m2 and 2.1 mW
m2 for green light (in 1999 and 2000, respectively). In
pre-spring 1999, the birds were also tested under bright red light with a
higher intensity of 43x1015 quanta s1
m2 (condition RX; 13.0 mW m2). Control
tests (C) took place under `white' light produced by an incandescent light
bulb with an intensity of approximately 24 mW m2.
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For the tests in the above-mentioned C, R, RX and G conditions, the birds
were caught in their housing cages shortly before the `white' room light went
off and were put immediately into the test cages. Birds that were to be tested
after pre-exposure to red light were moved for the period of these tests into
a smaller room that was lit during daytime by fluorescent lamps. Roughly 1 h
before this white light went off, a red light with a peak wavelength of 635 nm
and an intensity of 3.1 lux (15 mW m2), produced by
brilliant red LEDs, was added to the white room light; after the white light
went off, the birds were exposed to the red light alone for approximately 1 h
before their tests under red (conditions RpeR and RpeRX) or green (condition
RpeG) light began. During spring 2000, we also tested birds after pre-exposure
to total darkness for 1 h. These birds stayed in their housing cages after the
room lights went off; approximately 1 h later, they were caught in darkness,
put into the test cages and tested under red or green light (conditions DpeR
and DpeG, respectively).
Test apparatus and performance
Orientation behaviour was recorded in funnel cages
(Emlen and Emlen, 1966) lined
with typewriter correction paper (BIC, Germany; formerly Tipp-Ex), where the
birds were tested one at a time (see W. Wiltschko and Wiltschko,
1995
,
2001
). Each funnel cage was
placed in an aluminium cylinder, the top of which consisted of the plastic
disk carrying the LEDs. The light passed through at least two sets of
diffusers before it reached the bird. The light intensity in the test cages
was measured as irradiance using Optometer P9710-1 (Gigahertz-Optik, Puchheim,
Germany) with the radiometric probe `Visible' RW-3703-2, a silicium
photoelement for the wavelength range 400800 nm.
Recording in conditions C, R, RX and G began in the evening at about the
time when the light went off in the housing cages; those in conditions with
pre-exposure to red light or darkness began 1 h later (see above). The
tests lasted
75 min. When active, the birds left scratch marks on the
coating of the inclined walls that documented the distribution of their
activity. The birds were tested three times in each condition involving red or
green light; in the control condition, they were tested up to five times.
Data analysis
After removal from the cage, the coated paper was divided into 24 sectors,
and the scratch marks in each sector were counted. Recordings with a total of
<35 scratches were excluded from the analysis because of too little
activity (see W. Wiltschko and Wiltschko,
1995 for details).
From the distribution of the activity within the cage, the heading and the
concentration of the respective test were calculated. From the headings of a
bird under each condition, we calculated the mean vector of that bird, with
the direction b and the length rb. The
b of the 12 or 16 birds tested were comprised in the grand
mean vector for each condition, with the direction
N and the
length rN. The grand mean vectors were tested by the
Rayleigh test for significant directional preferences. The orientation in the
various conditions was tested by the non-parametric Mardia Watson Wheeler test
for differences in distribution
(Batschelet, 1981
) and by the
MannWhitney U-test applied to the differences of the birds'
mean headings from the grand mean to test for differences in variance.
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Results |
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Effect of pre-exposure to red light on the orientation response under red light
The tests in pre-spring 1999 focussed on the question of whether
orientation under red light could be induced either by increasing the
intensity of the red test light sixfold or by pre-exposure to red light.
The mean headings of the test birds and the grand mean vectors are given in
Fig. 1. Under 635 nm red light
of both light levels tested, the birds were disoriented. After pre-exposure to
red light, however, robins were significantly oriented in the migratory
direction under red light of both light levels pre-exposure to long
wavelengths enables robins to obtain directional information under these long
wavelengths (see Möller et al.,
2001). The orientation under red light was indistinguishable from
the behaviour under control conditions; under bright red light, the birds
showed a significant increase in scatter compared with the control, but their
directional preference was still significant.
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Additionally, birds that had been pre-exposed to red light were tested under green light (see Table 1, upper section, RpeG); these data are included in Fig. 2 as open symbols.
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Comparing pre-exposure to red light with pre-exposure to total darkness
The tests in pre-spring 2000 focussed on the processes by which
pre-exposure to red light induced the orientation under red light. Did
pre-exposure to red light stimulate the receptors underlying the orientation
under red light or not? If not, pre-exposure to red light should be equivalent
to total darkness for these receptors that, as a result, might become more
sensitive, enabling them to extract enough information from the
short-wavelength end of the red LED spectrum to indicate directions. To check
this possibility, we compared the effect of pre-exposure to red light with
that of pre-exposure to total darkness. Additionally, we tested the birds
under 565 nm green light to see whether the two types of pre-exposure also
affected the behaviour at other wavelengths.
The results are given in Fig. 2. Under red light, the birds were once more disoriented, while under green light they were excellently oriented in the northerly migratory direction. Pre-exposure to red light led to oriented behaviour under red light as before, whereas a similar exposure to total darkness failed to induce an oriented response, with the behaviour not different from that under normal red light (P>0.05, Mardia Watson Wheeler test).
The birds were also tested under green light after both types of
pre-exposure. Pre-exposure to darkness did not affect the orientation under
green light, while pre-exposure to red light did not alter the general nature
of the response but appeared to increase the scatter (see
Table 1). The pooled data of
1999 and 2000 are significantly oriented (23 birds:
N=357°, rN=0.53, P<0.01,
Rayleigh test) but also show significantly more variance than the joint
control sample (P<0.01, MannWhitney test).
Seasonal change in headings between spring and autumn
Responses to certain light regimes in Australian silvereyes (Zosterops
l. lateralis) and European robins had turned out to be fixed responses,
not changing between autumn and spring (W. Wiltschko et al.,
2000,
2003
,
2004
). To check whether the
induced orientation under red light showed the normal seasonal reversal, we
tested birds in autumn, with tests under white and green light serving as
controls.
The results are given in Fig. 3. The robins tested under red light after pre-exposure to red light preferred the seasonally appropriate southerly directions, with their behaviour not different from that under white or green light (P>0.05, Mardia Watson Wheeler test).
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Discussion |
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Here, magnetite-based magnetoreception comes to mind. Crystals of magnetite
have been found in numerous animals (see
Kirschvink et al., 1985;
R. Wiltschko and Wiltschko,
1995
). In birds, they are located in the ethmoid region and in the
upper beak (e.g. Beason and Brennan,
1986
; Williams and Wild,
2001
; Fleissner et al.,
2003
). However, behavioural data
(Beason and Semm, 1996
;
Munro et al., 1997
) as well as
electrophysiological recordings (Semm and
Beason, 1990
) indicate that magnetite-based receptors do not
provide birds with directions but with a different type of information: they
appear to detect magnetic intensity used as a component of the navigational
`map'. Attributing the compass orientation observed in our experiments to
magnetite would thus be at variance with these findings. Electrophysiological
responses of neurons in the nBOR to changes in magnetic north in the presence
of red light beyond 600 nm (Semm and
Demaine, 1986
), on the other hand, show that the light-dependent
system is also active in the long-wavelength range. In view of this, our
present findings strongly suggest that red light with a peak wavelength of 635
nm or 645 nm can, in principle, mediate the detection of magnetic
directions.
Change in receptors or different receptors?
The observation that an increase in intensity to a sixfold level did not
lead to orientation indicates that the reason for the disorientation normally
observed under red light is not the light intensity being below threshold. The
ability to orient under red light obviously depends on previous exposure to
the same or similar wavelengths. The fact that exposure to total darkness
failed to elicit oriented responses clearly shows that the birds' ability to
extract information from the magnetic field under long-wavelength light is not
based on the receptors becoming more sensitive when not stimulated. It is the
pre-exposure to red light that affects the receptive system in some way that
leads to the detection of magnetic direction under conditions where it is
normally not possible.
One possibility is that red light changes the absorption spectrum of the
receptor(s), causing a shift towards longer wavelengths by activating a second
absorption peak in the long wavelength range, a phenomenon reported for
certain pigments in plants. Photopigments with two absorption peaks have also
been described in the parietal eye of lizards
(Solessio and Engbretson,
1993) and are considered for salamanders by Phillips and
Deutschlander (1997
). The
other possibility is that a second receptor with a peak at longer wavelengths
is involved and provides the information for the newly gained orientation
ability.
Electrophysiological recordings from the nBOR have indicated two types of
neurons responding to changes in magnetic directions, one with a peak
absorbance near 503 nm and the other with a peak absorbance near 582 nm
(Semm and Demaine, 1986). This
implies two different receptors as the origin of the information transmitted
by these neurons. Also, the very abrupt transition from oriented behaviour
under green light to disoriented behaviour under yellow light
(Wiltschko and Wiltschko,
1999
; Muheim et al.,
2002
), as well as the unexpected responses of birds to a
combination of yellow and short-wavelength light
(W. Wiltschko et al., 2004
),
can hardly be explained by one receptor alone. Hence, the assumption of a
second type of receptor activated by longer wavelength light appears more
likely.
Red light produces a different response pattern?
Why would birds be able to use information provided by this long-wavelength
receptor only after they had experienced red light? The analysis of the avian
magnetic compass revealed what appears to be a similar phenomenon with respect
to magnetic intensities (W. Wiltschko,
1978): magnetic compass orientation was found to be narrowly tuned
to the intensity of the ambient magnetic field, with an increase or decrease
of only
25% leading to disorientation; exposure to fields outside this
range, however, enabled birds to orient under higher or lower intensities
obviously, birds could now interpret previously unreadable magnetic
fields. Interestingly, this newly gained ability seems to be limited to
intensities that the birds had directly experienced: robins normally living at
46 000 nT and now exposed to 150 000 nT were able to orient at 46 000 nT and
150 000 nT but not at the intermediate intensity of 81 000 nT
(W. Wiltschko, 1978
).
The radical pair model of magnetoreception
(Ritz et al., 2000) provides
an explanation for this phenomenon: the processes mediating magnetoreception
would result in specific patterns of activation across the retina, which are
centrally symmetric to the axis of the magnetic field lines. Their size and
pattern would vary with changing magnetic intensities. Hence, an abrupt
increase or decrease in intensity would suddenly confront birds with a novel
pattern, which might confuse them at first, resulting in disorientation.
However, because the altered pattern would retain the central symmetry with
respect to the axis of the field lines, the birds could learn to interpret the
novel pattern and thus regain their ability to detect magnetic directions.
Interpreting the induced ability to orient under red light as an analogous
case would mean that red light alone causes a pattern of response on the
retina that differs markedly from the one produced by white light or by light
from the bluegreen part of the spectrum. Yet this pattern, too, would
necessarily be centrally symmetric to the axis of the field lines, and this
might enable birds to learn to derive directional information from it.
The interpretation that the induced ability to orient under red light is
caused by the birds becoming able to interpret a novel response pattern raises
the question of why the pattern produced by red light alone should be
initially unreadable. It implies that it must somehow differ from the patterns
produced by the bluegreen part of the spectrum or the combined pattern
of both types of receptors under white light. This means that in the combined
pattern, the part produced by bluegreen light would dominate, as
indicated by the birds' ability to orient at once when tested under
monochromatic blue, turquoise and green light (e.g.
W. Wiltschko et al., 1993; W.
Wiltschko and Wiltschko, 1999
,
2001
). Red light would seem to
produce the minor, complementary component of the joint pattern. Both patterns
seem to act in a functionally synergistic way, providing birds with the same
type of information. The abrupt change from orientation to disorientation
around 570 nm (Wiltschko and Wiltschko,
1999
; Muheim at al.,
2002
), on the other hand, appears to suggest an antagonistic
interaction.
A spectral system as described for salamanders?
For amphibians, the other vertebrate group with a light-dependent magnetic
compass, antagonistic interactions between two spectral components located
either in the same or in two different receptors have been proposed
(Phillips and Deutschlander,
1997; Deutschlander et al.,
1999a
). The available data suggest parallels, but also interesting
differences, between the magnetic compass mechanisms of amphibians and
birds.
In salamanders heading shoreward, the spectral range where monochromatic
light produces the same responses as white light is considerably narrower than
in birds, ending at 450 nm (Phillips
and Borland, 1992
), in contrast to 565 nm in birds. The most
important difference between the two groups, however, concerns the behaviour
under long-wavelength light: from 500 nm onwards, the headings preferred by
the salamanders shifted by
90° counterclockwise with respect to those
recorded under white light (Phillips and
Borland, 1992
; Deutschlander et
al., 1999b
). Salamanders that were kept under long wavelengths and
had a chance to establish the shoreward direction under these light conditions
preferred the true shoreward direction under red light but showed the reverse
90° shift when tested under white light. These observations seemed to
imply that the directional information perceived under long-wavelength light
differed from that under white or blue light. The authors speculate about two
antagonistic spectral mechanisms indicating directions perpendicular to each
other (see also Phillips and
Deutschlander, 1997
;
Deutschlander et al., 1999a
).
At 475 nm, where both mechanisms would be equally stimulated, the salamanders
were disoriented (Phillips and Borland,
1992
). To reconcile this finding with the normal orientation
observed under white light, where both mechanisms are likewise activated,
Phillips and Deutschlander
(1997
) postulate that the
short-wavelength part of the spectrum produces a stronger stimulus that
dominates under full-spectrum light. Still, one would normally argue that a
mechanism producing what would seem false information would be selected
against. In view of this, Phillips and colleagues (Philllips and Deutschander,
1997; Deutschlander et al.,
1999a
) propose that this second mechanism might be an intrinsic
component of the magnetoreceptive system and discuss photopigments with two
absorption peaks, as described in the pineal of lizards
(Solessio and Engbretson,
1993
), as possible receptors.
These findings clearly contrast with the disorientation normally observed
in birds under yellow and red light at intensities of 6x1015
quanta s1 m2 or higher
(W. Wiltschko et al., 1993;
W. Wiltschko and Wiltschko,
1999
; present study). Muheim et al.
(2002
), testing birds in
autumn under red light of only
3x1015 quanta
s1 m2, i.e. about half the intensity of
that used in the present study, observed a westerly tendency that was
different from the southerly migratory direction and which they interpreted as
a shift in direction. Tests in spring, however, showed that this is
misleading: the birds also headed west (271°, 0.52, P<0.05; W.
Wiltschko and R. Wiltschko, unpublished), indicating that the response under
dim red light is independent of the migratory direction; rather than a shift
in compass direction, it appears to be a `fixed direction' similar to the
response observed, for example, in silvereyes under high-intensity green light
(W. Wiltschko et al., 2000
,
2003
). This argues against a
model such as the one proposed for amphibians. The response of robins to a
combination of yellow light with green or blue light
(W. Wiltschko et al., 2004
)
likewise suggests that the interactions between the short-wavelength and the
long-wavelength receptor in birds are far more complex than the model for
amphibians suggests. The most important difference to salamanders, however, is
the nature of the induced response under red light: birds show the same
directional tendencies as under white light. The amphibian system of two
mechanisms providing what would seem disagreeing information, perpendicular to
each other, thus has no parallel in birds. Birds pre-exposed to red light
oriented alike under red light and green light, with the induced orientation
under red light showing the typical seasonal change, identifying the behaviour
as true migratory orientation.
Another difference between amphibians and birds is the site of
magnetoreception: in salamanders, magnetic directions are mediated by
extraocular photoreceptors in the pineal
(Deutschlander et al., 1999b),
whereas magnetoreception in birds takes place in the eyes, in particular in
the right eye (W. Wiltschko et al.,
2002a
). In view of this, marked differences in the type of
receptors and in the way the receptors are connected with higher order units
are not surprising.
A possible role of the minor component
Nevertheless, because birds can spontaneously orient under monochromatic
short-wavelength light, but not under red light, we must also conclude that
the long-wavelength mechanism provides the minor component of the combined
pattern activated by white light. The biological function of this second
component is not yet clear, in particular because both components appear to
indicate the same directions.
The argument about a possible role of two spectral mechanisms in birds must
consider that, while the information provided by both mechanisms is
essentially the same, suggesting synergistic interactions, the sharp
transition from orientation to disorientation around 570 nm indicates
antagonistic interactions. To reconcile these seemingly contradictory
findings, we can only speculate. For example, the type of second receptor
might limit the area of the activation induced by the magnetic field in order
to make the magnetic compass more precise a possible analogue to
lateral inhibition, as it is found to enhance the contrasts in the visual
system. The size of a potential pattern of activation by magnetoreception in
the eye is not known; the pictures given by Ritz et al.
(2000) are purely arbitrary.
Behavioural evidence from migrants that were repeatedly tested in cages
indicate individual vectors based on 68 headings of
0.9 (data from
Wiltschko et al., 1998
,
2002b
). Considering the
circumstances of the tests, this implies a very high accuracy of the avian
magnetic compass. Mechanisms improving the precision of magnetic compass
readings thus do not appear unlikely, and the long-wavelength receptors would
serve an important function in the magnetoreceptive system of birds.
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Acknowledgments |
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References |
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