Waved albatrosses can navigate with strong magnets attached to their head
1 Fachbereich Biologie, University of Oldenburg, D-26111 Oldenburg,
Germany
2 Department of Biology, University of Missouri-St Louis, St Louis MO
63121-4499, USA
3 Department of Psychology, Queen's University, Kingston, Ontario, Canada
K7L 2Y1
4 Department of Biology, Wake Forest University, Winston-Salem, NC
27109-7325, USA
* Author for correspondence (e-mail: henrik.mouritsen{at}uni-oldenburg.de)
Accepted 6 August 2003
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Summary |
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Key words: waved albatross, Phoebastria irrorata, navigation, magnetic orientation, satellite telemetry
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Introduction |
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In contrast to the relatively large number of studies on magnetic compass
orientation in night-migrating songbirds (e.g. Wiltschko and Wiltschko,
1972,
1995a
,
1996
;
Mouritsen, 1998
), we do not
presently know which compasses homing pelagic seabirds use. We do know that
homing pigeons Colomba livia use a sun compass
(Schmidt-König, 1961
;
Schmidt-König et al., 1991; Chappel,
1997
; Wallraff et al.,
1999
) and probably also a magnetic compass (e.g.
Keeton, 1971
; Walcot and
Green, 1974; Visalberghi and Alleva,
1979
; Wiltschko and Wiltschko,
1995a
), even though magnetic compass orientation in homing pigeons
has been difficult to replicate (e.g.
Lamotte, 1974
;
Moore, 1988
). It has also been
suggested that magnetic cues may be used by homing pigeons as the basis for an
extrapolated `map-sense' (for reviews, see
Walcott, 1991
;
Wiltschko and Wiltschko,
1995a
). However, the cues used by homing pigeons during the
map-step of the map and compass model (Kramer,
1953
,
1957
) are a source of constant
controversy.
Many pelagic seabirds face the problem of finding a small island in the middle of a vast ocean that seems to provide no visual landmarks. Migration and homing over open ocean, therefore, seem to present seabirds with some of the most difficult orientation and navigation challenges faced by any type of bird.
Since the late 1980s, satellite transmitters communicating via the
Argos satellite system have been commercially available to avian researchers
(Jouventin and Weimerskirch,
1990), but since these transmitters and the associated satellite
time are very expensive, they have, until now, been used primarily for
conservation purposes to elucidate where threatened or endangered populations
forage, breed and winter (e.g. Robertson
and Gales, 1998
; Tickell,
2000
). However, satellite telemetry also has great potential for
studying the orientation responses of freely migrating birds, particularly for
individuals whose access to hypothesized orientation cues has been
manipulated. Unfortunately, the tendency of many seabirds to travel and forage
in unpredictable directions away from their breeding colonies makes detecting
effects of navigational cue manipulations difficult.
Waved albatrosses breed almost exclusively on Isla Española,
Galápagos, Ecuador, and during the incubation period they typically
make direct trips to the up-welling zone off the coast of Perú, ca.
1300 km from Galápagos (Anderson et al.,
1998,
2003
;
Fernández et al., 2001
;
see also Figs 2,
3,
4). Throughout most of the
60-day incubation period, both male and female breeders alternate incubation
stints with long foraging trips lasting about 20 days. Birds making these long
trips fly along straight paths to and from the foraging area. This
straight-line flight path pattern has so far been observed using satellite
tracking in nine tracks of long-trip flights taken by seven different
individual non-manipulated adult incubating waved albatrosses (combining data
from Anderson et al., 1998
, and
two additional individuals from this study). In addition, 19 trips from seven
different chick-rearing birds followed by satellite in 1996 showed a broadly
similar pattern (Fernández et al.,
2001
; Anderson et al.,
2003
). The straight-line nature of their routes and high
predictability of their destination during the incubation period make waved
albatrosses an ideal species for seabird navigation studies, since deviations
from their intended flight paths caused by manipulated orientation cues can be
easily detected.
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The aim of our study was to test whether access to the undisturbed geomagnetic field is crucial to the orientation and navigation capabilities of waved albatrosses. We used satellite telemetry to compare flight paths of magnetically manipulated albatrosses with those of controls.
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Materials and methods |
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Satellite transmitters and location data
We tracked a total of 14 incubating albatrosses in 2000 and an additional
seven incubating albatrosses in 2001. In both 2000 and 2001, incubating birds
were temporarily removed from the nest and 30 g Platform Transmitter Terminals
(PTTs; Microwave Telemetry Inc., Columbia MD USA) were sewn to Tesa tape (Tesa
Tape, Inc., Charlotte, NC 28209, USA) feather `sandwiches' constructed on
their backs (see additional details in
Fernández, 1999;
www.wfu.edu/~djanders/PTTmount.jpg).
These birds were then tracked using the satellites of the Argos System
(Service Argos, Largo, MD, USA). The transmitters themselves produce only
negligible magnetic disturbances (see Table
1). Since the distance between the transmitter and the head of the
albatross was 30-33 cm when flying, the magnetic disturbances from the
transmitter were about one order of magnitude smaller than the natural daily
variations in the geomagnetic field (bold numbers in
Table 1).
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In 2000, two PTTs transmitted continuously, and five PTTs transmitted on an
8 h:24 h on:off duty cycle to conserve battery power. All PTTs used in 2001
operated on a continuous transmission cycle since the conservative 8 h:24 h
on:off cycle was too limiting on the number of positions that we could
collect. The girth of the Earth at the equator also limits the number of
satellite views of the PTTs (Service Argos user manual, v.1 1988, Landover,
MD, USA) so that the average number of contacts (including classes 3, 2, 1, 0,
A and B) in this study was 0.22-0.73 locations per PTT per day (mean 0.54) for
the conservative duty cycle and 1.42-3.73 locations per day (mean 2.52) for
the continuous duty cycle. To maximize data collected, we used six of seven
location quality classes provided by Argos (all but class Z), as in previous
studies (Anderson et al., 1998;
Fernández et al.,
2001
). Ground-truthing conducted at the site in 1995 showed that
the lowest quality locations that we used, Class B, had a mean error of 17.8
km (9.6 nautical miles; Anderson et al.,
1998
).
Geomagnetic field manipulation equipment
Attaching a strong, permanent magnet to a bird is a commonly used way of
depriving free-flying birds of information from the undisturbed geomagnetic
field (for a review, see Wiltschko and
Wiltschko, 1995a, p. 160). To
examine the effects of magnetic field manipulation on waved albatrosses, we
glued a 3.5 g neodymium-iron-boron magnet to the back of the head of ten
incubating albatrosses. We also glued a 0.05 g neodymium-iron-boron magnet to
each bird at the proximal end of the culmen's dorsal surface. Brass (`sham')
pieces of similar mass and size (3.5±0.5 g and 0.05±0.01 g),
which did not affect the magnetic field, were attached in the same manner to
nine other incubating adults. The birds were assigned semi-randomly to
treatment group, so that the first two birds included one magnet and one sham
bird, the next two, one magnet and one sham bird, and so on. Within each set
of two birds, the assigned treatment order was randomized taking into account
the sex of the birds, so that the sexes were also evenly represented in each
group. In addition, we tracked the flights of two untreated controls (no head
attachments) to confirm that the albatrosses still used the same routes and
foraging areas as in 1995 (Anderson et al.,
1998
). The seven tracks from incubating birds followed in 1995
provide seven additional control tracks from five different individuals.
The 3.5 g (ca. 4.5 g together with the epoxy embedding) magnet imposes a stationary magnetic field stronger than 100,000 nT (100 000 nT=1 Gauss) within 10 cm of the magnet. The direction of this field depends on the orientation of the magnet. We oriented the large magnets so that each added a horizontal magnetic component of at least 100 000 nT to the entire head of the albatross, including the proximal 1.7 cm of the beak. The horizontal magnetic field disturbance was still greater than 30 000 nT as far as 14 cm from the magnet, which includes the nares, located at most 12 cm away from the large magnet. Using our attachment method, the magnetic compass disturbance was maximized at the suggested magnetic sensory locations including the eyes and the nasal region, since the resultant magnetic field vector (found by adding the Earth's field to the magnet's field) will always point in approximately the same horizontal direction relative to the head of the bird independent of the bird's bearing. Furthermore, it is important to realize that the geomagnetic field strength and direction stay constant in the geographical frame of reference, whereas the field produced by the stationary magnets glued to the bird follows the movement of the bird's head. Therefore, the strength of the resultant field sensed by the bird will constantly change up to 60 000 nT (± the strength of the geomagnetic field) when the bird moves its head.
The 0.05 g (ca. 0.08 g with the epoxy embedding) magnet imposes a
stationary magnetic field stronger than 50 000 nT, 25 000 nT and 5000 nT to
volumes larger than 2 cm, 3 cm and 5 cm in radius, respectively, around the
magnet. We placed the small magnet at the dorso-proximal end of the bill to
ensure that the proposed magnetite-mediated magnetoreceptor in the nasal
region (Walker et al., 1997;
Walker, 1998
;
Williams and Wild, 2001
;
Kirschvink et al., 2001
) was
blocked from obtaining meaningful magnetic information, even if the large
magnet was lost.
Exposing migratory songbirds to a strong magnetic pulse designed to disturb
the magnetization of single-domain magnetite crystals deflected their
orientation, but did not, at least in some cases, seem to impair their ability
to pick a consistent compass direction
(Beason et al., 1995; Wiltschko
et al., 1994
,
1998
;
Wiltschko and Wiltschko,
1995b
). Given these data, it has been suggested that the proposed
magnetite-mediated magnetoreceptor in the nasal region is involved in sensing
magnetic map cues rather than magnetic compass cues
(Wiltschko et al., 1998
). We
therefore oriented the small magnets so that they changed the horizontal
component of the magnetic field (and thereby the inclination) as much as
possible. Around the magnetic equator, the total field strength is ca. 30 000
nT and the inclination is close to 0°. Magnetic inclination changes
approximately 2° per 1 geographical degree moved on the north-south axis
around the magnetic equator. Thus, a change of just 1000 nT in the vertical
magnetic component is equivalent to a north-south displacement of one
geographical degree [inv tan(1000/30000)=2° inclination=1 geographical
degree] equal to 111 km. Consequently, even small changes of the vertical
magnetic component imposed by our stationary magnets should lead to loss of
homing ability in waved albatrosses if they use a magnetic map to
navigate.
Magnet and sham attachment and nest monitoring
We monitored sets of 35 (2000) and 42 (2001) nests with daily visits,
beginning at nest initiation in late April and early May of 2000 and 2001 and
continuing until nests were assigned to a treatment category. We discontinued
monitoring unassigned nests after all treatment categories were filled.
Satellite transmitters and magnets or brass shams were attached after 9-20
days of incubation to 12 incubating albatrosses (six of each treatment) in
2000 and seven birds (four magnet and three sham) in 2001. We attempted to
deploy gear on birds at the end of a typical incubation stint to increase the
chances that the bird left the colony shortly after attachment of equipment,
thereby saving battery power. All birds left the colony between a few hours
and 8 days post-deployment.
During attachment of satellite transmitters and magnets or shams, individuals were placed in a canvas bag and restrained gently in the investigator's lap. The bird's head was passed through an opening at the distal end of the bag to isolate the head during gear attachment and to decrease potential thermal or respiratory stress. All birds were released at their nests within 20-40 min of capture. To attach the rear treatment or sham, a small circle of skin on the back of each manipulated or sham bird's head was exposed by clipping away the feathers. Magnet or brass pieces embedded in hardened epoxy resin were glued to the exposed skin using a thin layer of Vetbond (3M, www.3m.com) for the initial group of six birds. Several small feathers were cut away from the area at the feather-culmen interface at the proximal end of the bill and the smaller magnets and shams were glued into the small pocket created by the clipped feathers.
Despite numerous successful laboratory tests with the initial Vetbond attachment method, the first three magnet birds and the first three sham birds returned from their trip without head attachments. In the second and subsequent rounds of attachment, the rear-mounted magnet and brass pieces were glued with epoxy resin to the non-adhesive side of strips of Tesa tape (4 cm long) 1-2 days prior to attachment. We sandwiched several head feathers between the Tesa tape-treatment piece and a second piece of Tesa tape, affixing this to the exposed skin using a layer of Vetbond directly on the skin as a protectant, and several drops of a cyanoacrylate glue (Duro Super Glue, Manco, Inc., Avon, OH, USA) over the Vetbond and adjacent feathers to adhere the treatment to the bird. Following this modification, three birds returned with both magnets still attached, and four additional birds returned with the front magnet only. After removing the equipment from birds returning with magnet or brass pieces still in place, we treated the exposed skin with Betadine as a precaution to avoid infection, although we detected no broken skin or sign of infection in any bird carrying a magnet or sham. All procedures were approved by animal care and use committees in Canada and the US and by the Charles Darwin Research Station in Galápagos.
To complement the satellite data collected to document routes, trip duration and ground speed of the traveling birds, we visited the nest of each bird twice daily, at 06:00 h and 18:00 h, recording the identity of the incubating bird and the disposition of the gear, if applicable. Additional notes were recorded whenever we passed through this part of the colony at other times of the day.
Incubating adults remain at their nest or in small areas adjacent to their nesting territories when on land (K. P. Huyvaert, unpublished data), so we can safely assume that our birds were still at sea if they were not found in the study subcolony. The satellite data strongly supported this assumption in all cases in which the satellite transmitters were still attached and functioning properly on return. Therefore, both the satellite data and the twice-daily searches enabled us to collect accurate total trip length duration data.
Tracking data and meteorological correlates
For all birds fitted with continuous duty cycle transmitters, we calculated
the resultant (straight line) traveling speed of the albatrosses seen over a
period of approximately 24 h during their outward and homeward travel. In
practice, this was done by calculating the fastest recorded straight-line
speed between two satellite fixes, which were recorded at least 20 h apart.
Data from birds fitted with conservative duty cycle transmitters proved too
sparse to properly evaluate traveling speeds.
During the entire tracking period, we monitored the cloud cover at each bird's location by downloading weather satellite images (See example in Fig. 1; http://goes-8-gems.cira.colostate.edu) at 3 h intervals. The satellite images were calibrated by comparing the corresponding satellite image with careful local cloud cover observations made 5 times daily during the experiment at Española and during an airline flight between the Galápagos and mainland Ecuador on 24 July 2000. In 2000, the cloud cover was generally minimal during the entire period of testing, which is atypical for the season. In 2001, the weather was more typical for the season; cloudy conditions mixed with sunny periods dominated.
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Results |
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The albatrosses in this study, regardless of treatment, tended to use a more southerly route on the home journey from the South American coast to Galápagos than they used during their outward journey from Galápagos to the South American coast (Figs 2, 3, 4). Furthermore, the return trips were made at higher straight-line ground speeds than were the outbound trips: for trips with enough reliable satellite fixes to calculate straight-line ground speeds during both journeys, outward and homeward speeds averaged 23±3 km h-1 and 30±5 km h-1, respectively (within subject comparison: paired t-test: t=-2.941, d.f.=6, P=0.026; considering only birds returning with at least one magnet/sham in place: outward speed, 23.5±2.7 km h-1, homeward speed, 29±5 km h-1; within subject comparison: paired t-test: t=-2.337, d.f.=5, P=0.067). Given this difference between outward and homeward ground speeds, we analyzed performance during the two journeys separately.
Treatment groups did not differ in several estimates of performance (Fig. 5). (1) Total trip length (all birds considered: one-way ANOVA: P=0.92 and pair-wise comparison between magnet and sham birds: t-test, t=-0.337, d.f.=16, P=0.74; considering only birds returning with at least one magnet/sham in place: one-way ANOVA: P=0.84 and pair-wise comparison between magnet and sham birds: t-test, t=-0.447, d.f.=9, P=0.67; considering only birds returning with the large magnet/sham in place: one-way ANOVA: P=0.71 and pairwise comparison between magnet and sham birds: t-test, t=0.393, d.f.=3, P=0.72); (2) outward speed, all birds considered: mean outward speed=23 km h-1 for both magnet and sham birds (t-test, t=0.0, d.f.=8, P=1.00); considering only birds returning with at least one magnet/sham in place: mean outward speed=24 km h-1 for magnet birds and 26 km h-1 for sham birds (t=-0.735, d.f.=5, P=0.495); (3) homeward speed, (all birds considered: mean homeward speed=30 km h-1 for magnet birds and 28 km h-1 for sham birds (t-test, t=0.518, d.f.=5, P=0.627); considering only birds returning with at least one magnet/sham in place, mean homeward speed=30 km h-1 for magnet birds and 28 km h-1 for sham birds (t=-0.408, d.f.=4, P=0.704); and (4) route (see Figs 2, 3, 4).
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To further test if the birds' ability to locate Galápagos in a vast
ocean was affected by the attached magnets, the straightness of the return
paths was evaluated by comparing the orientation of each section (at least 100
km long) of the return journey relative to the true home direction
(Fig. 6). In this analysis, we
included only birds returning with at least one magnet/sham in place and for
which we have at least five reliable (class B or better) satellite fixes. The
expected mean direction from the Peruvian upwelling zone to Galápagos
was 308°, and both magnet and sham birds were very well-oriented in the
correct homeward direction (magnet birds: N=26 track sections,
=307°, r=0.89, P<0.001; sham birds:
N=14 track sections,
=310°, r=0.85,
P<0.001). The magnet birds in fact showed slightly less
directional scatter during the homeward trips than did sham birds. Thus adult
waved albatrosses, even with strong stationary magnets attached close to their
proposed magnetic sensory locations, showed no signs of reduced navigational
abilities. Figs 2,
3,
4,
5,
6 and
Table 2 summarize the
results.
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Cloud cover varied during trips (Table 2). The cloud scores in Table 2 are conservative, because when the satellite images were compared with local observations at Espanõla, birds homing under cloud score `3-2' probably encountered completely overcast conditions. However, a few holes in the cloud cover cannot be excluded for any trip. Thus, all we can safely say is that both magnet and sham birds were able to home during predominantly cloudy conditions.
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Discussion |
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Since we were conducting this study on a protected species with a limited distribution, we wanted to ensure that no animal would suffer from any long-term effects even if the magnets had a major effect on their orientation capabilities. To do this, we used a non-permanent attachment method designed to ensure that all magnets would fall off within 1-2 months, so that experimental animals would be able to regain their orientation and navigation capabilities in case the treatment had a dramatic effect on the birds' ability to find their way. Furthermore, we used attachment methods that did not impair the birds' feeding capabilities and could be easily removed without harming the birds when they returned with the attachments still in place. Subcutaneous placement of the magnets/shams was not a feasible option. Consequently, our attachment method was chosen as the best balance between the risks of losing the equipment prematurely and potential long-term effects on the subjects.
Of the 10 magnet birds, seven individuals returned with the small magnet still in position and three birds returned with the large magnet still in place (see Table 2). Of the nine sham birds, four individuals returned with the small sham still in place and two birds returned with the large sham still in place. After fixing the magnets/shams, some birds stayed on their eggs for several days (up to 8) and they all retained their gear while in the colony. The birds that did lose the gear before returning probably did so when they had got to Perú and subjected the gear to saltwater and other foraging stresses. It is likely that most, if not all, birds carried both magnets/shams at least during the outward trip to the Peruvian coast. In any case, whether all birds were considered, or only those returning with the magnets still in place, no significant or suggestive differences were observed with respect to delay before departure, total trip duration, outward straight-line flying speed, homeward straight-line flying speed, straightness of homeward journey, or large-scale route chosen.
Since four out of ten magnet birds returned with only the small magnet in place, it is relevant to discuss the disturbances in the Earth's magnetic field produced by the small magnet alone in relation to the proposed sensory mechanisms in the eyes and the nasal region. The head anatomy of the albatross means that the small front magnet will have imposed significant disturbances to the earth's magnetic field in the nasal and eye region, even if the large magnet was lost. The small magnet imposes an additional artificial field of strength 50 000 nT, 25 000 nT and 5000 nT at distances of 2, 3 and 5 cm, respectively, from the magnet. The distance (in cm) from the front magnet position (1) to the centre of the eyeball was 4.0 (males), 3.8 (females); (2) to the outer surface of iris, 3.3 (males), 2.9 (females); (3) to a point in mid-skull between the two irises, 2.7 (males), 2.6 (females); and (4) the diameter of eyeball, 2.0 (males), 1.9 (females). Even a change of 5000 nT in the vertical component would lead a bird using a magnetic map and relying at least partly on measuring inclination (the most reliable north-south magnetic parameter) to determine its position approximately 5 geographical degrees or ca. 555 km too far north or south of its actual position. Changes of 5000 nT or 25 000 nT in the horizontal component would make birds using a magnetic compass choose bearings that were off by up to 9.5° and 40°, respectively. Thus, even on their own, the small magnets would have produced significant disturbances in the magnetic field around the proposed magnetic sensory locations in the albatrosses' eyes and/or nasal region.
Can we be sure that magnetic field disturbances produced by stationary magnets completely inhibit birds' ability to obtain useful orientation information from the geomagnetic field? Below, we separately evaluate the theoretical influence of stationary magnets on magnetoreception for both the hypothesised magnetite-mediated and light-mediated sensory mechanisms.
Magnetite-mediated receptor, magnetic compass cues
When a stationary magnet positioned on the bird's head produces an
additional horizontal magnetic field stronger than the Earth's field, the
waved albatrosses cannot use any magnetite-mediated magnetic compass located
in the head region, because a magnetite crystal will be affected by the total
resultant field vector, and magnetic fields are vector fields. The resultant
field vector is found by adding the magnetic field vectors from the attached
magnets to the geomagnetic field vector. Consequently, if the horizontal
disturbance from the stationary magnet is stronger than 30 000 nT (the
approximate strength of the geomagnetic field around the Equator), the
resultant magnetic vector stays in one half of the circle, for instance from
west through north to east, so that no southern vector component ever exists,
regardless of the geographical direction in which the albatross's head is
pointing. Consequently, if birds use a magnetite-mediated magnetic compass,
attaching a strong stationary magnet near the sensory location will prevent
the bird from obtaining useful compass information from the Earth's magnetic
field. For the same reasons, the possibility that waved albatrosses use
magnetite-mediated magnetosensing to assemble outward journey information in a
path integration strategy can also be excluded.
Light-mediated receptor, magnetic compass cues
As mentioned above, positioning a stationary magnet adding a field stronger
than 30 000 nT to the head of a bird (for the large magnets, the artificial
field at the eyes is much stronger than 100 000 nT) means that the resultant
magnetic vector stays in one half of the circle (or even less) regardless of
the geographical heading of the bird. At first glance, logic would lead one to
conclude that such a compass would be dysfunctional no matter how the compass
information is perceived. However, it could be argued that if birds use a
radical-pair, light-mediated, magnetoreception mechanism
(Ritz et al., 2000), they may
be able to use the geomagnetic field as a compass even in the presence of a
strong stationary magnet, since the ghost images hypothesised by Ritz et al.
(2000
) may still be modulated
in a regular fashion. If that is the case, birds would, however, have to adapt
to a completely new set of patterns. This would take some time and, more
importantly, the birds would have to calibrate this novel pattern to another
geographical frame of reference before it would be of use to them. We doubt
that the albatrosses in this study had sufficient time to do this before they
left the colony.
Light-mediated receptor, magnetic map cues
For theoretical reasons, birds using a light mediated, quantum-chemical
mechanism are only able to sense the direction and gross strength of the total
field, not the small modulations in intensity required for a magnetic map, and
the currently suggested light-mediated mechanisms can therefore be excluded as
magnetic map-senses.
Magnetite-mediated receptor, magnetic map cues
First of all, the evidence that birds can make use of minute gradients in
the Earth's magnetic field strength and/or inclination to establish a
magnetically based map is limited
(Wiltschko and Wiltschko,
1995a). In fact, some researchers in the field challenge the
validity of all evidence suggesting any involvement of a magnetic map-sense in
pigeon and other bird navigation (e.g. Wallraff,
1999
,
2001
). For birds to derive
positional information that is precise enough to locate a small island in a
vast ocean, from a magnetic map-sense, they would need to sense their position
relative to gravity with high precision whilst also, in flight, detecting
minute changes in the geomagnetic field's intensity (see e.g.
Wallraff, 1999
). If birds do
have a magnetic map-sense, it must either rely on inherited magnetic
parameters (which would then have to be based on fixed absolute values) or
must be acquired by experience.
If a magnetic map-sense is based on measuring absolute values of magnetic parameters, a stationary magnet placed close to the sensory organ will obviously make it dysfunctional. If a magnetic map were instead acquired by experience, it could be plastic and/or based on relative values, and it could be argued that a stationary magnet might not interrupt the correct sensing of relative values, but remember that the magnetic field strength continuously varies up to 60 000 nT depending on the albatross's head orientation. Even if birds are able to deal with this highly unnatural situation, positional feedback from other cues facilitating a complete recalibration of the birds' map would be a prerequisite. Does a bird at the Peruvian upwelling zone have positional feedback available that would enable it to recalibrate all its magnetic map-values for use on its first journey after attachment of stationary magnets? That would require the birds to know/guess that the new `magnetic anomaly' observed prior to leaving the colony is consistent all over the range covered by their magnetic map. We find that hard to believe.
Furthermore, any magnet glued to skin will be moving relative to any sensory location(s) inside the head of the bird, since the skin of waved albatrosses (and other birds) is not rigidly fixed to the skull. Consequently, even the most subtle movements of the stationary magnets relative to the sensory organ will be likely to produce magnetic disturbances too large to enable the bird to reliably sense the minute differences in the magnetic parameters needed to use the geomagnetic field as a map-cue.
Preliminary data (Haugh et al.,
2001) from conditioning experiments with homing pigeons,
Columba livia, suggest that pigeons can be trained to discriminate
(rather poorly; 60-70% success rate) between two opposite directions based on
a magnetic anomaly after a stationary magnet had been attached to their head.
Are such results from conditioning experiments relevant to the interpretation
of our albatross data? Birds in a conditioning experiment get direct feedback
(in the form of a food reward) on how they should interpret the occurrence of
a completely new magnetic field after application of a strong stationary
magnet to their head. Therefore, adding a magnet to a bird's head in a
conditioning experiment is merely a separate type of conditioning experiment.
By contrast, no direct feedback is available to a wild free-flying bird trying
to navigate over open ocean. Therefore, this type of conditioning experiment
seems inadequate to answer the question of whether strong stationary magnets
prevent free-flying navigating birds from obtaining useful information from
the geomagnetic field.
Regardless of how birds may perceive magnetic fields, if our waved albatrosses needed to recalibrate a magnetic compass or a magnetic map, one would expect the magnet birds to stay in the colony longer than the sham birds prior to departure. This is not the case. In fact, one magnet bird left the colony within just 5 h, and no significant differences in time to departure between magnet and sham birds were observed (P=0.65, see Results). Alternatively, if important navigational information had been disturbed, we expected that birds would not leave the colony or that they would feed in close proximity to the colony. Such behaviour by the magnet birds was not observed.
The ability of birds to home, orient and/or navigate with strong stationary
magnets glued to their head has previously been found in homing pigeons and a
few other species under mostly sunny conditions (for a review, see table 6.2
in Wiltschko and Wiltschko,
1995a). Our results agree with these findings. The only previous
data from seabirds showed that Cory's shearwaters Calonectris
diomedea could home over short distances (<400 km) with stationary
magnets attached to their head, neck and wings
(Massa et al., 1991
) and that
the trip lengths of black-browed albatrosses Diomedea melanophris
were unaffected by the attachment of strong magnets
(Bonadonna et al., 2003
).
Given that the albatrosses in our study seem to have successfully navigated
with strongly disturbed magnetic orientation cues, what other cue(s) could
they have used to guide their open ocean navigation? The obvious compass
candidate is the sun compass (Kramer,
1953; Schmidt-Koenig, 1961;
Schmidt-Koenig et al., 1991
).
We did not observe reduced homing speed or increased trip length during cloudy
conditions (see Table 2), yet
it is difficult to be absolutely sure whether sun compass cues were available
from holes in the clouds when, according to the satellite images, conditions
appeared to be completely overcast. Therefore, we cannot exclude the
possibility that the tracked birds had a sun compass available, at least
irregularly, during all journeys reported here.
The waved albatrosses in our study may also have been aided partly by
olfactory cues (Wallraff,
2001), particularly since the olfactory bulbs of procellariiforms
(petrels, shearwaters and albatrosses) tend to show strong hypertrophy. The
olfactory bulbs occupy up to 37% of the total brain volume in pelagic seabirds
compared to ca. 3% in most other birds (Bang,
1966
,
1971
). Olfactory cues could
provide map-like cues enabling seabirds to determine their position relative
to home (Wallraff and Andreae,
2000
) or they may provide a beacon-cue attracting birds to their
destination.
In conclusion, our study shows that waved albatrosses are able to navigate between two well-known locations 1300 km apart along straight and predictable routes with strong magnets attached to their heads. Even though we find it unlikely that our albatrosses had access to any useful magnetic information, if their sensory organ is located in the head region, the definitive interpretation of these results depends on the magnetic sensing mechanism used by birds, and this is currently not known. So, while we cannot rule out that magnetic cues play a role in albatross navigation under natural conditions, our study does provide new, hard-to-obtain data from wild, free-flying birds performing non-forced natural navigational tasks in specifically manipulated magnetic fields, against which future empirical and theoretical findings related to the magnetic sensory mechanism of birds can be evaluated.
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