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First published online February 15, 2008
Journal of Experimental Biology 211, 649-653 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014183
Food intake and fuel deposition in a migratory bird is affected by multiple as well as single-step changes in the magnetic field
1 Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden
2 Swedish Museum of Natural History, Bird Ringing Centre, Box 50 007, SE-104 05
Stockholm, Sweden
* Author for correspondence (e-mail: ian.henshaw{at}zoologi.su.se)
Accepted 2 January 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: geomagnetic cues, bird migration, food intake, fuel deposition
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) and external information about migratory direction
(Alerstam, 1990;
Berthold, 1996). The migratory
journey requires birds to store energy in the form of fat accumulated at
stopover sites along the migration route
(Blem, 1990). Most migrants
store relatively small amounts of fat (<25% of lean body mass) and
regularly refuel at successive stopover sites
(Alerstam and Lindström,
1990). Nevertheless, large ecological barriers such as the Gulf of
Mexico or the Sahara desert require large fuel loads for a successful crossing
(Berthold, 1993). Migratory
flights over the Sahara desert involve distances of at least 1500 km, and
birds can double their mass (100% increase relative to lean body mass) by
storing fat prior to crossing the desert
(Fry et al., 1970). Mostly,
endogenous mechanisms have been thought to control various aspects of a
migrant's physiology and behaviour including both timing and amount of
fuelling during migration (Berthold,
1996). Recent evidence now strongly suggests that temporal and
spatial precision of bird migration incorporates additional external cues
along with the inherited migratory program
(Fransson et al., 2001;
Thorup and Rabøl, 2001;
Jenni and Schaub, 2003;
Fransson et al., 2005;
Alerstam, 2006;
Kullberg et al., 2007). In
order to find confined species-specific areas it seems likely that birds must
use some additional external cues in combination with clock-and-compass
orientation (Fransson et al.,
2005).
Both celestial cues (e.g. Emlen,
1970; Able, 1982;
Moore, 1987) and information
from the Earth's magnetic field are known to be used by birds to determine and
maintain migratory direction (Wiltschko
and Wiltschko, 1995). Beck and Wiltschko
(Beck and Wiltschko, 1988)
showed that hand-reared juvenile pied flycatchers (Ficedula
hypoleuca) use the magnetic field to trigger directional changes,
suggesting that they respond to changing magnetic field values or perhaps
values specific to a geographic position. Orientation responses of adult
Australian silvereyes (Zosterops l. lateralis) subjected to
experimental manipulations of the magnetic field simulating displacements
along the migration route indicate that they may use the magnetic field as
part of a navigational map in order to find their wintering area
(Fischer et al., 2003).
Evidence for physiological reactions to geomagnetic cues in migratory birds
come from studies of fuelling decisions in two migratory species, the thrush
nightingale (Luscinia luscinia)
(Fransson et al., 2001;
Kullberg et al., 2003) and
European robin (Erithacus rubecula)
(Kullberg et al., 2007).
Fransson et al. (Fransson et al.,
2001) and Kullberg et al.
(Kullberg et al., 2003)
exposed first-year thrush nightingales to four successive changes in magnetic
field parameters, simulating a migratory journey from Sweden to northern
Egypt, where extensive fuelling could be expected prior to passage over the
Sahara desert. Experimental birds showed increased fuel deposition rate
compared to control birds remaining in the ambient magnetic field of southeast
Sweden.
In preparation for migration, many birds develop a state of hyperphagia or
over-eating (e.g. King, 1961;
Bairlein, 1985), and together
with an increased efficiency of food utilization
(Bairlein, 1985;
Klaassen and Biebach, 1994),
this provides an important mechanism for migratory fuelling. The cause for the
observed increase in body mass in response to a simulated geomagnetic field
remains, however, to be determined.
To investigate the significance of food intake on the body mass changes
observed in the earlier studies (Fransson
et al., 2001; Kullberg et al.,
2003) in the work reported here we analyze food intake of the
nightingales. Furthermore, to study whether a single shift in magnetic field
value is sufficient to provide information for fuelling decisions we performed
a new experiment, exposing thrush nightingales trapped in Sweden, directly to
a magnetic field of northern Egypt. If birds use the successive change in the
magnetic field experienced during a natural migration for fuelling decisions,
we would expect experimental birds directly exposed to the magnetic field of
Egypt to show similar amount of food intake and fuel deposition rate as
control birds experiencing the ambient magnetic field of southeast Sweden.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Birds were randomly assigned to either a treatment group, experiencing a
manipulated magnetic field implemented by a magnetic coil system, or to a
control group experiencing only the ambient magnetic field and surrounded by a
wooden dummy coil. The magnetic coil system consisted of two independent
series of four quadratic coils each, arranged orthogonally
(Lohmann and Lohmann, 1994).
For technical details of the magnetic coil system see Kullberg et al.
(Kullberg et al., 2003).
Each coil system (magnetic or dummy) was placed in a shed built of non-magnetic materials and placed 15 m apart. Within each coil system, birds were placed individually in four separate cages, separated by sound absorbing baffles. Semi-transparent plastic roofs prevented access to potential celestial cues. Each shed had two daylight bulbs (HP1-T Plus Philips Powertone 400 W; Philips Sweden AB, Stockholm) following the natural daylight to compensate for the reduction in light spectra caused by the plastic roofs.
Control birds experienced no manipulation of the magnetic field and
remained in the ambient magnetic field of Tovetorp, southeast Sweden
(58°56'N, 17°08'E; total intensity: 50 800 nT,
inclination: 72°20') during the 11 days of the experiment.
Experimental birds were exposed to a magnetic field of northern Egypt
(31°00'N, 29°00'E; total intensity: 43 200 nT,
inclination: 45°10') during the 11 days of the experiment. This
experiment was replicated twice, birds in the first replicate started on the
5th August ±2 days, and birds in the second replicate started on the
18th August ±3 days. These dates correspond to the early and the late
phases of the onset of autumn migration for thrush nightingales, respectively
(Kullberg et al., 2003). Thus
a total of 16 birds were used in the experiment, eight received the magnetic
treatment, experiencing the geomagnetic field of northern Egypt, and eight
experienced no manipulation but remained in the ambient magnetic field of
southeast Sweden. In order to record body mass of the birds, food trays were
attached to electronic scales (Precisa 310C, Precisa Gravimetrics AG,
Dietikon, Switzerland) connected to computers, enabling automatic registration
of body mass (to 0.01 g) for each bird. Body mass increase was calculated
using weights at time 19:30 h.
The study was carried out with permission from the Swedish Animal Welfare Agency (permission no: 26-02).
Recording of food intake in the present experiment and the earlier experiments
In both the present experiment (2004) and the earlier experiments in 2000
and 2001 (Fransson et al.,
2001; Kullberg et al.,
2003) birds were fed daily with a mixture containing meal worms
(Tenebrio molitor; 30 g) and dry food (10 g)
(Berthold et al., 1990) and
given water ad libitum. For each bird the amount of food remaining in
the trays was weighed daily. The difference between the amount fed and
remaining was used to calculate food intake.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In experimental birds, body mass increase was equally high between early and late season replicates whereas control birds showed a lower body mass increase during the course of the experiment in the early season replicate compared with the late season replicate (Table 1, Fig. 1).
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The effect of magnetic field change on food intake
Birds trapped early in the season in all three years differed in food
intake; experimental birds had a higher food intake during the course of the
experiment compared with controls (Table
2, Fig. 2). Birds
trapped late, however, showed no difference in food intake between treatments
(Table 2,
Fig. 2).
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|
DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Kullberg et al., 2003)
(Fig. 3), birds directly
experiencing the magnetic field of northern Egypt, reached a high fuel load
irrespective of time of season, while control birds (experiencing the ambient
magnetic field in southeast Sweden) by contrast, gained higher fuel loads only
in the late replicate. This is in line with observations that birds late in
the migratory season are likely to be increasingly time constrained and
increase their fuel load (Fransson,
1998; Därnhardt and
Lindström, 2001; Kullberg
et al., 2003) and that late birds show a tendency to migrate with
higher speeds (Ellergren,
1993; Fransson,
1995; Schaub and Jenni,
2000a; Schaub and Jenni,
2000b). Our results thus confirm the earlier studies on thrush
nightingales suggesting that migratory birds can use information from the
Earth's magnetic field during migration for fuelling decisions
(Fransson et al., 2001;
Kullberg et al., 2003).
Furthermore it indicates that nightingales do not require a successive change
in magnetic field in order to incorporate magnetic information into their
migratory program.
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Nevertheless, whether the effect shown is triggered by any latitudinal change or is a response evolved to a specific area where a large fuel load is needed remains to be investigated. Evidence so far suggesting that experienced adult birds might use magnetic map information to determine their relative position comes from orientation responses of Australian silvereyes (Zosterops l. lateralis). The birds under study showed the expected orientation responses when experimentally tested to changes of the magnetic field that simulated displacements to different locations along their migratory route (Fisher et al., 2003). Whether our manipulated nightingales use any change in the magnetic field as trigger signal to initiate weight gain, use geomagnetic cues to determine their position as a component of a bi-coordinate navigational map or whether they can also use regionally specific magnetic fields as signposts indicating important areas, such as prior to ecological barriers, or to locate their wintering and breeding areas, remains to be investigated.
Experimental birds in the early season replicate receiving either a
successive change in magnetic field
(Fransson et al., 2001;
Kullberg et al., 2003) or a
single-step change to a magnetic field of northern Egypt (this study) showed
higher food intake compared to control birds. Birds trapped late however,
showed no difference in food intake between experimental and controls. The
fact that the pattern of food intake in the experiments performed in all three
years was nicely reflected by observed body mass patterns
(Fig. 2) strongly suggests that
birds react to the magnetic treatment by increasing food intake, causing an
increase in fuel deposition. The increased energy and nutrient demands needed
for migratory fuelling are known to be mostly achieved through an increase in
food intake or hyperphagia (Bairlein,
2003), probably combined with an increase in assimilation
efficiency of food eaten (Bairlein,
1985; Bairlein,
1999). Furthermore our result is in line with earlier findings of
food intake and fuel deposition in migratory European robins. Robins showed
lower food intake and fuel loads when experiencing a magnetic treatment
simulating a migratory journey from Sweden to their wintering area in southern
Spain where their migratory fuel load is expected to decline
(Kullberg et al., 2007).
The physiological mechanism by which the manipulated magnetic field affects
nightingales to increase food intake remains to be investigated; however,
regulation of foraging behaviour is believed to be influenced by
corticosterone (e.g. Gray et al.,
1990; Long and Holberton,
2004), the primary glucocorticoid hormone in birds. Corticosterone
has recently been shown to affect foraging behaviour, lipid stores, migratory
activity and orientation behaviour in migratory birds
(Holberton et al., 2007;
Holberton, 1999;
Piersma et al., 2000;
Löhmus et al., 2003).
Recently Löhmus et al. (Löhmus
et al., 2006) observed that migratory red-eyed vireos (Vireo
olivaceus) treated with increased levels of corticosterone visited
feeding bowls more often than control birds. Corticosterone further correlates
with the stages of refuelling and flight and has been suggested to serve as a
cue when birds prepare to reinitiate flight at a stopover site
(Landys-Cianelli et al.,
2002). Our results thus suggest that geomagnetic information might
trigger hormonal changes in migratory birds enabling appropriate fuelling
behaviour during migration. Further investigation is, however, required to
determine the links between geomagnetic cues, hormones and feeding behaviour,
when birds are fuelling in preparation for a barrier crossing.
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Acknowledgments |
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