Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light
Bird Migration Group, Department of Animal Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden
* Author for correspondence (e-mail: rachel.muheim{at}zooekol.lu.se)
Accepted 17 September 2002
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Summary |
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Key words: migratory orientation, magnetoreception, magnetic compass, European robin, Erithacus rubecula
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Introduction |
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In birds, little is known about the number and possible interactions of the
magnetoreception mechanisms. The orientation of birds has been studied under
different wavelengths of light between 424 nm (blue) and 635 nm (red) and
under different intensities ranging from 0.57x1015 quanta
s-1 m-2 to 43x1015 quanta
s-1 m-2 (full-spectrum light excluded; see
Fig. 5). The experiments showed
that both juvenile and adult birds of different species were disoriented under
590 nm (yellow) and 630 nm (red) light but oriented into the seasonally
expected migratory directions under full-spectrum (white), 424 nm and 443 nm
(blue), 510 nm (turquoise) and 565 nm (green) light
(Wiltschko et al., 1993;
Wiltschko and Wiltschko, 1995
,
1999
,
2001
;
Munro et al., 1997
;
Rappl et al., 2000
). Young
inexperienced pigeons were disoriented after being displaced under 630 nm
light but oriented towards the home direction after being transported to the
release site under 565 nm or full-spectrum light
(Wiltschko and Wiltschko,
1998
). These results indicate that magnetoreception capabilities
are disrupted under light of peak wavelengths longer than 565 nm.
Light-dependent magnetoreception has also been shown to vary between different
intensities of light of the same wavelength in the form of directional shifts
under higher light intensities (43-44x1015 quanta
s-1 m-2; Wiltschko et al.,
2000a
,b
;
Wiltschko and Wiltschko,
2001
). Australian silvereyes oriented during both spring and
autumn migration towards NW under high-intensity 565 nm light (Wiltschko et
al.,
2000a
,b
).
European robins that oriented towards the seasonally appropriate northerly
directions under 424 nm, 510 nm and 565 nm light at low intensities
(7x1015 quanta s-1 m-2) in spring
showed axial orientation into EW directions at high light intensities
(43-44x1015 quanta s-1 m-2) under 424
nm and 565 nm light, but unimodal north-westerly directions under 510 nm light
(Wiltschko and Wiltschko,
2001
).
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Three biophysical magnetoreception models have been proposed to explain the
light dependence of the magnetic compass in animals. They all meet the
necessary requirements for a magnetic inclination compass by showing axial
rather than polar characteristics and by being insensitive to changes in
magnetic intensity smaller than 10% of the geomagnetic field
(Deutschlander et al., 1999).
Leask's optical pumping model (Leask,
1977
) is based on a double resonance process that involves the
lowest excited triplet state of molecules such as rhodopsin in the retina. The
high frequencies (MHz) required for a resonance process to occur probably do
not exist in living systems and therefore Leask's model does not seem very
likely (Phillips et al.,
1999
). Schulten
(1982
) demonstrated that an
external magnetic field can influence photon-induced processes that involve
bimolecular reactions. In this process, radical pairs are formed by photon
excitation through light absorption similar to the photosynthetic reactions.
Based on this theory, Schulten and Windemuth
(1986
) proposed a model for a
biophysical magnetic compass with rhodopsin or iodopsin as likely organic
reactants. The animals would perceive the magnetic field as an apparent
variation in light intensity or colour in their visual field. Recently, this
magnetic compass model was refined by Ritz et al.
(2000
) and a newly discovered
class of photoreceptors, the cryptochromes, were proposed as the
magnetosensors. It was shown theoretically that magnetic fields with
intensities in the range of the geomagnetic field can produce a significant
increase of the triplet yield, which also depends on the relative orientation
between the magnetic field and the radical pairs
(Ritz et al., 2000
). Edmonds
(1996
) developed a model for a
sensitive magnetic compass that detects magnetic field information optically
through ferro(i)-magnetic crystals, such as magnetite, located in the oil
droplets of the avian retina. According to his model, freely moving magnetite
particles located in the oil droplets interact with large dye molecules such
as ß-carotene and align parallel to the geomagnetic field, letting light
enter to specialized photoreceptors when the position of the bird's head is
oriented parallel or antiparallel to the geomagnetic field lines
(Edmonds, 1996
).
To study the light dependence of the magnetic compass of passerine birds,
we carried out orientation cage experiments with juvenile European robins
exposed to 560.5 nm (green), 567.5 nm (green-yellow) and 617 nm (red) light at
three different intensities (1 mW m-2, 5 mW m-2 and 10
mW m-2). We used lights with a half bandwidth (/2) of only
9-11 nm. These wavelength ranges were much narrower than the ones used in
previous orientation studies on birds performed under monochromatic light (in
other studies,
/2 ranged from 30 nm to 70 nm). Thus, we could examine
in more detail the function of the magnetoreception mechanism in the expected
transition zone between oriented and disoriented behaviour around 565 nm light
under three different intensities.
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Materials and methods |
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An IL1700 Research Radiometer (International Light, Newburyport, MA, USA) with a detector SHD033 (range 3x10-8-1x10-2 W m-2, spectrum 200-1100 nm) was used to measure overhead light intensity inside the orientation cages, at the level of the birds' head in the middle of the orientation cage at 65 mm height, under the same number of opaque Plexiglas sheets as used during the experiment. The readings were recalculated into radiometric irradiance (mW m-2) and photon quantities (photon irradiance: quanta s-1 m-2, log quanta s-1 cm-2) for each colour used (Table 1). The light intensity was adjusted so that the lights inside the cages had approximately the same radiometric irradiance, regardless of wavelength and bandwidth. With a calibrated S2000 spectrometer (Ocean Optics Inc., Dunedin, FL, USA), we measured the spectrum of the full-spectrum and monochromatic light between 300 nm and 800 nm passing through one opaque Plexiglas sheet. In addition, we measured the full-spectrum light passing through differently strong ND filters and multiple layers of opaque Plexiglas sheets, but we could not find substantial deviations in the spectral composition between the various combinations of diffusers and/or ND filters.
We used six automatic, funnel-shaped registration cages (diameter 30 cm,
height approximately 15 cm, overhead view 160°) with eight circularly
arranged plates connected to micro-switches, which registered the birds'
migratory activity (for one plate, only one activation per second was allowed;
Fig. 1). These automatic
registration cages give results comparable with data from experiments with
funnel cages lined with typewriter correction paper
(Emlen and Emlen, 1966) and
have extensively been used in orientation experiments with passerine birds
(e.g. Sandberg et al., 1988
;
Åkesson, 1993
).
Experimental procedure
A total of 36 juvenile European robins (Erithacus rubecula
Turdidae) was tested between the beginning of October and the beginning of
November 2001. The birds were caught at Ottenby Bird Observatory (56°
12' N, 16° 24' E), Sweden during their first autumn migration
and were transported to Stensoffa Ecological Field Station (55° 42'
N, 13° 25' E), Southern Sweden. The birds were kept indoors in
individual cages under the natural light regime, but without access to visual
cues outdoors, for a maximum of 38 days. The birds were provided with
mealworms and vitaminized water ad libitum. After an acclimation
period of 3-6 days, in which the birds were allowed to adjust to living in a
cage, we first recorded the birds' orientation behaviour between one and three
times under full-spectrum light (W20 bc) at an irradiance of
79x1015 quanta s-1 m-2 (see
Table 1) in order to let the
birds accustom to the experimental situation. All experiments took place
during the evening hours, with the first of a maximum of three groups starting
approximately one hour before sunset. The birds were allowed an adjustment
period of 5-10 min after being placed into the orientation cage, before their
activity was registered during a period of 60 min. Each bird was tested only
once per evening.
After the initial experiments under full-spectrum light, each bird was tested once under each colour and intensity (see Table 1), starting with 5mW m-2 (14-16x1015 quanta s-1 m-2), continuing with 10 mW m-2 (29-32x1015 quanta s-1 m-2) and 1 mW m-2 (2.9-3.2x1015 quanta s-1 m-2) and ending with a final experiment under 5 mW m-2. The order of colours under which each individual bird was tested was random. Some individuals were tested twice under one experimental condition if the first experiment did not reveal a valid result, mainly due to low activity (see below for conditions). The control experiments under full-spectrum light at an irradiance of 3.9x1015 quanta s-1 m-2 (W1), 79x1015 quanta s-1 m-2 (W20 ac) and 39x1015 quanta s-1 m-2 (W10) were performed at the end of the experimental series in the given order. The experiments took place in the natural geomagnetic field of approximately 50 µT and an inclination of 70° (declination 1.5°; WMM 2000, 15 October 2001).
Statistical analyses
The registrations recorded in the orientation cages were analysed with
standard procedures described by Batschelet
(1981). For each active bird
that activated the micro-switches at least 40 times, we calculated an
individual mean direction (
) and an individual mean vector length
(r). The mean direction was analysed for axiality by using the method
of doubling the angles (Batschelet,
1981
). If the axial mean vector length (r2) was
larger than the unimodal vector (r), the experiment was considered
axial and the end of the axis closer to the unimodal direction was included in
further analyses. An experiment was considered to be valid when the individual
mean vector length corresponded to r
0.05. Only the first valid
experiment per bird, colour and intensity was included in further analyses, so
each individual was represented only once in each experimental group.
The mean direction of a group was analysed using circular statistics
(Batschelet, 1981). Differences
in directions between experimental groups were tested for significance using
the oneway classification test (F1,df;
Mardia, 1972
). Only groups
with unimodal distributions significantly different from random according to
the Rayleigh test were compared.
Statistical differences in mean number of registrations and mean individual
vector length between the three colour experiments of the same intensity or
the three intensities within one colour were analysed using the nonparametric
KruskalWallis test. Differences between proportions of valid
experiments and unimodal versus axial individuals were analysed using
the 2-test.
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Results |
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Discussion |
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A light-dependent magnetoreception system based on antagonistically
interacting, magnetically sensitive spectral mechanisms has been described in
Eastern red-spotted newts (c.f. Phillips and Borland,
1992a,b
).
Normal orientation was recorded under wavelengths of
450 nm, 90°
shifted orientation was recorded under wavelengths of
500 nm, and
disorientation was recorded under an intermediate wavelength of 475 nm. In
conclusion, light-dependent magnetoreception in these newts seems to be
mediated by one spectral mechanism in the shorter wavelengths below 450 nm and
by another spectral mechanism in the longer wavelengths above 500 nm. An equal
excitation of both mechanisms leads to disorientation, suggesting that the two
wavelength mechanisms interact antagonistically with each other (for a review,
see Deutschlander et al.,
1999
). There is evidence that the short-wavelength mechanism is
more sensitive than the long-wavelength mechanism in amphibians (J. Phillips,
personal communication), leading to a system where even a small amount of
short-wavelength light can equalize or override the input from the
long-wavelength mechanism. Our data support the existence of a similar system
in birds, with a short-wavelength mechanism in the blue-green part of the
spectrum and a long-wavelength mechanism in the red part of the spectrum.
Seasonally appropriate migratory orientation under 560.5 nm
light
Our European robins oriented, directionally very concentrated, towards
southwest or axially towards southwestnortheast under 560.5 nm light.
The southwesterly direction corresponds to the expected migratory direction.
Our birds were in good migratory condition, with high mean fat values
(5.7±1.0, mean fat score ± S.D., according to the eight-grade
fat scale by Pettersson and Hasselquist,
1995) and high mean body mass (17.9±1.4 g) in the middle of
the experimental period. We can therefore assume that the birds exhibited true
migratory behaviour. Also, other orientation studies on wavelength-dependent
magnetoreception with different species of birds consistently showed oriented
behaviour towards the seasonally expected migratory direction under green
light (peak wavelength 565 nm) at intensities of approximately
6-8.7x1015 quanta s-1 m-2 and shifts in
orientation or axial behaviour under higher light intensities (for a
discussion on the effects of light intensities, see below; see
Fig. 5 for an overview;
Munro et al., 1997
;
Rappl et al., 2000
; Wiltschko
et al.,
2000a
,b
).
A magnetic inclination compass was shown to be the underlying mechanism
because birds reversed their orientation when tested under green light in a
magnetic field with an inverted vertical component
(Wiltschko et al., 2001
). The
magnetoreception system of birds thus seems to behave in the same way under
green light of approximately 560/565 nm as under natural situations when
tested under natural skies during migration. In general, orientation has been
shown to be more concentrated under 560/565 nm light than under full-spectrum
light (c.f. this study; Wiltschko et al.,
1993
; Wiltschko and Wiltschko,
1995
; Munro et al.,
1997
; the only exception is the study on garden warblers by
Rappl et al., 2000
). These
observations indicate that green light excites a magnetically sensitive
mechanism to a higher degree than other wavelengths or the full spectrum and
that the avian magnetoreception system is very sensitive in the
short-wavelength region around green.
Disorientation under 567.5 nm light
Our birds were disoriented under light with a peak wavelength of 567.5 nm
at all intensities tested. This stresses the observation that magnetoreception
is indeed dependent on specific wavelengths of light. The very abrupt
transition from significant mean orientation towards the expected migratory
direction under 560.5 nm to disorientation under 567.5 nm strongly favours the
theory of a magnetoreception system based on two or several antagonistically
interacting spectral mechanisms with at least one activity peak in the
short-wavelength area below 567.5 nm and one activity peak in the
long-wavelength area above 567.5 nm. Equal excitation of two such mechanisms
by 567.5 nm light can, in theory, cause the sharp transition from oriented to
disoriented behaviour. The involvement of one spectral mechanism alone would
result in a more gradual transition between orientation and disorientation
over a much broader range of wavelengths due to the characteristics of
spectral sensitivity curves. There is a strong parallel between our results
and the disorientation found in Eastern red-spotted newts under the
intermediate wavelength of 475 nm (Phillips and Borland,
1992a,b
),
except that the wavelengths involved are shifted to the longer spectrum in our
case. In the newt system, equal excitation of both the short-wavelength
mechanism revealing normal orientation and the long-wavelength mechanism
producing a 90° shift in orientation results in disorientation. So, if the
disorientation of our European robins under 567.5 nm is comparable with the
disorientation in the newt system, there should be an antagonistic
long-wavelength mechanism at wavelengths of >567.5 nm. In conclusion,
testing birds under light of >567.5 nm should result in oriented behaviour,
shifted by approximately 90° relative to the control direction.
Shifted orientation under 617 nm light
Consistent with these predictions, our European robins were well oriented
under 617 nm light at the lower two intensities. Relative to the direction
chosen under 560.5 nm, the birds showed a 62° clockwise shift towards west
at the lowest intensity, R1. This shift is smaller than the
expected 90° shift (95% interval of the mean direction under 617 nm does
not include the expected 90°-shifted direction; see
Table 2). We can speculate that
the magnetic field provides information on the cardinal directions only under
monochromatic light of long wavelengths and that additional information from
other cues (for example, celestial cues) would be necessary for fine-tuning in
order to be able to identify the seasonally appropriate migratory direction.
If this was true, the westerly direction observed under red light
(R1) would correspond to a 90° shift from the magnetic south
direction.
Orientation experiments with four species of passerine birds as well as
displacement experiments with homing pigeons conducted under 590 nm yellow
light and 630-635 nm red light all resulted in disoriented behaviour (one
exception was observed by Möller et
al., 2001, see below; Fig.
5; Wiltschko et al.,
1993
; Wiltschko and Wiltschko,
1995
,
1998
,
1999
,
2001
;
Munro et al., 1997
;
Rappl et al., 2000
). The
apparent contradiction between our results and the previous findings can be
explained by the difference in the half bandwidth and maybe also in the peak
wavelengths of the light that the birds were exposed to. The yellow and red
lights produced by light-emitting diodes (LEDs) and used in previous
experiments not only have much broader wavelength spectra at 50% bandwidth
(
/2=33-43 nm) than the red light we used (
/2=9-11 nm) but also
become even broader at their bases (bandwidth at 1% peak transmission;
Wiltschko et al., 1993
;
Wiltschko and Wiltschko, 1995
,
1998
,
1999
,
2001
;
Munro et al., 1997
;
Rappl et al., 2000
;
Möller et al., 2001
). The
spectra of our monochromatic lights have a bandwidth at 1% peak transmission
of 21-30 nm; thus, they also have a very small bandwidth at their bases. Light
of a broad bandwidth is more likely to excite more than one spectral
mechanism, and a sensitive mechanism can become excited by very little light
from the outer edges of a spectral curve. Thus, in the case of an
antagonistically interacting system between spectral mechanisms with peaks at
different wavelengths, disorientation is more likely to occur under
broad-spectrum light. As already mentioned, we have indications that the
short-wavelength mechanism is more sensitive than the long-wavelength
mechanism in European robins. So, the left tail of the spectrum of the broad
red LED light could have excited a part of the right tail of the more
sensitive short-wavelength mechanism, leading to an equal excitation of both
mechanisms and disrupting the magnetoreception capabilities.
Previous orientation experiments under red light revealed significant
orientation into the expected migratory direction under one experimental
situation (Möller et al.,
2001). In that experiment, European robins, pre-exposed to red
light in their holding cages before the start of the experiment, were
significantly oriented when tested under red light. The control birds that did
not experience a red pre-exposure were disoriented when tested under red
light. For pre-exposure, red light was added to the normal full-spectrum light
in the holding house 2-3 h before the start of the experiment. One hour before
the experiments started, the full-spectrum light was switched off and the
birds were exposed to the red light only
(Möller et al., 2001
).
These experiments also suggest that birds are, in principle, able to orient
under long-wavelength light. Why, in the case of Möller et al.
(2001
), acclimation seems to
be necessary for a successful use of red light for magnetic compass
orientation is unclear.
Support for the involvement of a long-wavelength mechanism is also given by
neurophysiological studies, as presented in
Fig. 5. Extracellular
recordings in the nucleus of the basal optic root (nBOR) and in the optic
tectum in homing pigeons have resulted in responses to changes in the
direction of the magnetic field (Semm et
al., 1984) and peak magnetic responsiveness under wavelengths of
503 nm and 582 nm (Semm and Demaine,
1986
). The same cells also exhibited a response to magnetic
stimuli under 674 nm red light, thus responding to light of longer
wavelengths. However, these results have to be considered with some care
because of difficulties in repeating the experiment
(Deutschlander et al.,
1999
).
As we carried out our experiments indoors under controlled laboratory conditions, the birds were given access to geomagnetic information only. Further experiments under red light in a shifted or inverted magnetic field will show whether the reactions observed are true compass orientation or non-specific reactions towards a nonsense direction.
Orientation under different light intensities
Changes in orientation behaviour away from the expected migratory direction
have been observed at different light intensities in both European robins and
Australian silvereyes (Fig. 5;
Wiltschko et al.,
2000a,b
;
Wiltschko and Wiltschko,
2001
). The observed reactions, however, do not seem to be general,
but rather species-specific. Australian silvereyes reacted to higher
intensities of 43-44x1015 quanta s-1
m-2 (15 mW m-2) under 565 nm light by showing a shift
towards a fixed direction in the northwest during both autumn and spring
migration (Wiltschko et al.,
2000b
). European robins, on the other hand, preferred axial
eastwest directions under both 424 nm and 565 nm lights, but north to
north-westerly directions under 510 nm light at the same high intensity
(Wiltschko and Wiltschko,
2001
). The reason for the different reactions between Australian
silvereyes and European robins under the same intensity level remains unknown.
Our experimental birds also showed axial orientation, but at much lower
intensities (14x1015 quanta s-1 m-2)
compared with those reported by Wiltschko and Wiltschko
(2001
). The axial orientation
of our European robins was directed along the axis of the expected migratory
direction, thus indicating difficulties in identifying the correct axis rather
than a shift in orientation as shown in the European robins tested by
Wiltschko and Wiltschko
(2001
). At the highest light
intensity of 10 mW m-2 (29-32x1015 quanta
s-1 m-2), our birds were disoriented under both 560.5 nm
and 617 nm lights, which are the same wavelengths at which they were
significantly oriented under the lower two light intensities. Under 560.5 nm
light (G10), the disorientation observed is presumably a
statistical consequence of small sample size because the mean vector lengths
in the higher two intensities, G5 and G10, are almost
identical (r=0.41 and r=0.40, respectively) and the mean
directions of the birds point towards the same direction. Migratory activity
and motivation did not seem to be reduced between intensities of the same
colour light, as neither the percentage of valid experiments nor the mean
number of registrations or individual mean vector lengths were significantly
different among the three intensities (P>0.05). So, the ability to
perceive useful information for orientation or to interpret information and
transfer it into directed orientation behaviour must be impaired in some
way.
The disorientation under high-intensity 617 nm light can be explained by the proposed antagonistically working, high-sensitive short-wavelength and low-sensitive long-wavelength mechanisms. The low-intensity light preferentially excited the long-wavelength mechanism and only slightly stimulated the more sensitive short-wavelength mechanism. Increasing light intensity would favour the relative light input to the long-wavelength mechanism, as both our full-spectrum light and the one used by the Wiltschko group emit relatively more energy in the longer than in the shorter wavelengths (Fig. 2). However, with increasing intensity, the long-wavelength mechanism would become saturated or adapted, resulting in a relative decrease in sensitivity of the long-wavelength mechanism and in a relatively higher input to the short-wavelength mechanism until both mechanisms become excited equally, leading to disorientation.
According to the antagonistic wavelength-dependent magnetoreception
mechanism, any transition from directed orientation to shifted orientation
involving more than one spectral mechanism includes an intermediate state
where disorientation occurs. The relative excitation of a wavelength mechanism
revealing directed orientation and a wavelength mechanism revealing shifted
orientation, together with the sensitivity of the two mechanisms, decides on
whether a bird will be oriented into the expected direction, disoriented or
show a shift in orientation. Whether a mechanism becomes excited by a light
stimulus depends on whether the light spectrum of the stimulus overlaps with
the sensitivity spectrum of the mechanism. The magnitude of the excitation is
dependent on the number of photons received by the spectral mechanism, which
increases with increasing intensity. Thus, the discrepancies found between our
study and those of the Wiltschko group
(Wiltschko et al., 2000a;
Wiltschko and Wiltschko, 2001
)
can be explained by the different intensity levels and half bandwidths used in
the respective studies (see Fig.
5 for comparison).
Disorientation under full-spectrum light
In view of an avian magnetoreception system with antagonistically
interacting wavelength mechanisms, our full-spectrum light experiments allow
some very interesting conclusions. Our European robins were significantly
oriented only in the very first experiments under full-spectrum light at a
very high intensity (W20 bc). The westerly direction was
significantly different from G1 and does not coincide with the
expected migratory direction but is directed into the same direction as under
R1. The birds were disoriented in all the experiments under
full-spectrum light that were performed after the colour experiments.
The full-spectrum light we used in our experiments is supposed to reflect a
spectrum that is very close to natural outdoor conditions, and birds are
therefore expected to behave most naturally under full-spectrum light. A
spectral analysis of our full-spectrum light showed that the birds received
very little light from the UV spectrum below 400 nm and maximal light inputs
from approximately 760 nm in the near IR when tested under full-spectrum white
light (Fig. 2). Compared with
the spectrum of incandescent light bulbs used by others (e.g.
Wiltschko et al., 1993;
Munro et al., 1997
;
Rappl et al., 2000
;
Möller et al., 2001
), the
full-spectrum light emitted by xenon arc lamps matches the natural spectrum
better, and the emission of violet-blue light between 400 nm and 500 nm is
much higher (Fig. 2). So, it is
unlikely that our results are a methodological artefact. Contrary to this,
there are indications about the existence of a third spectral mechanism in the
UV-blue area at 400-450 nm, which could in our case have interfered with the
magnetoreception system in an antagonistic way. Directed orientation under 424
nm and 443 nm blue light has been reported by Wiltschko et al.
(1993
), Wiltschko and
Wiltschko (1999
,
2001
) and Rappl et al.
(2000
). Such an additional
spectral mechanism would have been activated to a much higher degree under the
full spectrum used by us than under a full-spectrum light produced by an
incandescent light bulb. Alternatively, the intensity peak measured in the
near IR around 760 nm of our full spectrum could have resulted in an
inappropriately high activation of the long-wavelength mechanism. Either one
could have resulted in an imbalance between the different, antagonistically
interacting spectral mechanisms (c.f.
Deutschlander et al., 1999
),
causing shifted orientation or disorientation in the same manner as argued
earlier, thus explaining the observed behaviour of our birds under
full-spectrum white light.
Our European robins were disoriented in all the experiments under
full-spectrum light that were performed after the colour experiments. The
significantly lower activity of the birds in the orientation cages might
explain the very bad orientation at the lowest intensity, W1, but
we would then also expect a lower proportion of active individuals and a
shorter mean individual vector length compared with the other experiments
performed under full-spectrum light. But why did our birds show shifted
orientation in the first experiment under full-spectrum light before the start
of the experiments under monochromatic light, but disorientation when tested
after the colour experiments? A possible explanation might be that changing
the spectral composition of light that the birds are exposed to could disturb
their ability to orient. This could be compared with the reactions observed
when changing the intensity of the ambient magnetic field
(Wiltschko, 1978). Orientation
experiments under magnetic fields of unfamiliar field intensity resulted in
disorientation until the birds adapted to the new situation after a few days
and learned to use the magnetic field information of unfamiliar field
intensity for orientation. In our case, a change of light conditions from
monochromatic to full spectrum rather than vice versa could have
confused the birds. This could explain why we got directed orientation under
full-spectrum light in our first experiments before the colour experiments
only.
In summary, in view of the idea of an avian magnetoreception system with antagonistically interacting wavelength mechanisms, the results obtained under full-spectrum white light are extremely interesting and they do not, in our opinion, disturb or reduce the importance of the results and conclusions from the colour experiments.
Biophysical processes of magnetoreception
Two theories are currently under discussion to explain the biophysical
processes of magnetoreception. The theory forwarded by Schulten and Windemuth
(1986) and Ritz et al.
(2000
) is based on radical
pairs, while the theory proposed by Edmonds
(1996
) is based on magnetite in
the birds' oil droplets. Both theories can theoretically build the
physiological basis for a magnetoreception system with two or more spectral
mechanisms. Directed orientation under red light seems to contradict the
magnetoreception model proposed by Ritz et al.
(2000
), as it assumes that
light of a specific minimum energy is needed to activate the biophysical
processes necessary for the detection of magnetic information. Cryptochromes,
a class of photoreceptors found in the avian retina and pineal gland
(Bailey et al., 2002
), with an
absorption spectrum in the blue and green wavelength range, were proposed to
be involved in light-dependent magnetoreception
(Ritz et al., 2000
). This,
however, does not exclude the possibility that other receptors with different
properties are involved in light-dependent magnetoreception. Molecules with
absorption spectra in the longer wavelengths of the spectrum could form a
long-wavelength mechanism, and antagonistic behaviour between the two
wavelength mechanisms could explain the abrupt cut-off between 560.5 nm and
567.5 nm light. Edmonds' model suggesting light-dependent magnetoreception in
combination with magnetite particles in the oil droplets of specialized
photoreceptors in the avian retina
(Edmonds, 1996
) can
theoretically also explain both the orientation under red light and the abrupt
behavioural change between 560.5 nm and 567.5 nm light. The cut-off filtering
effect of the oil droplets in the medium- and long-wavelength-sensitive
photoreceptors shifts the wavelength of peak absorbance of these
photoreceptors towards longer wavelengths (for example, 540 nm and 615 nm in
the canary, Serinus canaria, and 530-540 nm and 600-610 nm in the
Pekin robin, Leiothrix lutea) and also causes the effective spectral
sensitivity curves to fall off very steeply
(Maier and Bowmaker, 1993
;
Das et al., 1999
). We can
assume that the effective sensitivity spectra in European robins are similar.
Thus, photoreceptors exist that are sensitive in the medium- and
long-wavelengths, and, if inputs from such green and red photoreceptors are
processed as antagonistic signals, disorientation could occur at intermediate
wavelengths.
Ecological considerations
The question arises as to whether the observed properties of the birds'
orientation behaviour under different wavelengths and intensities of light
have an ecological explanation or whether the different reactions are based on
purely physiological reasons. Night-migrating birds are thought to select
their migratory direction at the time around sunset. Spectral irradiance
measurements at dusk show a relative increase of blue (peak at 450-500 nm) and
red (peak at 680 nm) light and a reduction in green, yellow and orange
(550-620 nm) light from daytime to twilight (see
Fig. 2. for comparison;
McFarland and Munz, 1975).
Thus, access to yellow-orange light is reduced during twilight, whereas blue
and red light is more intense. We can only speculate whether the limited
access to green light might be one reason for a higher sensitivity of the
short-wavelength mechanism in the green wavelength area compared with the less
sensitive long-wavelength mechanism in the red wavelengths and the possible
UV-blue mechanism. The disorientation of our birds under 567.5 nm light,
however, does not seem to be connected to the natural wavelength spectrum
during twilight. The light intensity levels used for the monochromatic light
in the various studies seem to cover a large range
(0.57-43x1015 quanta s-1 m-2; see
Fig. 5), but they all lie
within the intensities experienced under the natural twilight period for the
different wavelengths, as estimated from spectral irradiance curves measured
in nature during twilight (McFarland and
Munz, 1975
). McFarland and Munz
(1975
) performed their
spectral measurements in winter (30 January) and it is likely that the
spectrum and intensity of the light of an autumn sky is composed slightly
differently. Furthermore, differences in weather conditions, such as fog or
cloud cover, can have a large influence on the visible spectrum of the sky.
So, currently, it is difficult to find an ecological explanation for the
different reactions of the birds under different light intensities.
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