Migratory orientation of first-year white storks (Ciconia ciconia): inherited information and social interactions
1 Biological Station Rybachy, Rybachy 238535, Kaliningrad Region,
Russia
2 Max Planck Research Centre for Ornithology, Radolfzell 78315,
Germany
* Author for correspondence (e-mail: nchernetsov{at}bioryb.koenig.ru)
Accepted 19 December 2003
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Summary |
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Key words: orientation, white stork, Ciconia ciconia, spatiotemporal program, displacement
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Introduction |
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Juvenile white storks from East Prussia were detained in aviaries until all
free-living conspecifics had left the area and were then released. Recoveries
and subsequent sightings of experimental birds suggested that they generally
followed the southsoutheast (SSE) direction typical of white storks
migrating normally from East Prussia
(Schüz and Weigold,
1931). It was interpreted as evidence of the ability of young
inexperienced birds to find their winter quarters without receiving aid from
the adults, on the basis of an innate orientation mechanism
(Thienemann, 1931
; Schüz,
1949
,
1951
). However, as shown by
Wallraff (1977
) and using his
notation, where
is mean vector of recoveries and a is relative length
of the mean vector, so that a=1 means no directional variation and a=0 means
no directional preferences at all, the mean orientation of recoveries of the
delayed birds (
=170.3°, N=19, a=0.9395,
P<0.0001) slightly but significantly differed from the mean
orientation of recoveries of the non-manipulated birds from East Prussia
(
=159.3°, N=26, a=0.9737, P<0.0001; the
difference of 11° is significant at P<0.05: VWR test
(Batschelet, 1965
),
F=4.55; B test (Batschelet,
1972
), U=6.71; from Walraff, 1977). Furthermore, early
releases of East Prussian storks in western Germany (before the departure of
local experienced conspecifics) showed that the urge to follow other storks
dominates over inherited directional information
(Schüz, 1950
).
Later, similar experiments were performed in Latvia
(Katz, 1986). In the autumns
of 1970 and 1983, juvenile white storks were detained in aviaries until late
September, by which time all free-living storks had left Latvia. The mean
orientation of short-distance recoveries in the adjacent Lithuania was
192° (N=9), while the mean direction of recoveries at distances
greater than 400 km was 213° (N=5). The normal migratory
direction of Latvian storks within Europe is 168° (N=6). The
difference in migratory directions between the non-manipulated and the
experimental birds was significant (P<0.01, WatsonWilliams
test; Katz, 1986
).
Current theory suggests that inexperienced birds depart from their breeding
areas flying in a certain compass direction (Berthold,
1991,
1996
;
Mouritsen and Mouritsen,
2000
). After some time, they change their migratory direction, if
appropriate. Such spatiotemporal programming of migration brings the birds to
their population-specific wintering areas. This mechanism was shown by Gwinner
and Wiltschko (1978
) in their
experiment with hand-raised caged garden warblers, Sylvia borin, and
was demonstrated even more convincingly by Helbig et al.
(1994
).
In the light of these results, we suggested a hypothesis explaining the
more westerly mean direction of recoveries of detained white storks from East
Prussia (Thienemann, 1931;
Schüz, 1949
,
1951
) and from Latvia
(Katz, 1986
) as compared with
non-manipulated individuals. We assumed that the delayed storks made the
directional change that normally occurs at the Gulf of Iskenderun
(Berthold et al., 2001a
) at the
programmed date and took the southsouthwest (SSW) course while still in
Europe. However, the delayed birds differed from their non-manipulated
conspecifics in two respects: (1) they were travelling alone and could rely on
their innate orientation mechanisms only and (2) they were travelling late in
the season when their conspecifics had (nearly) reached the first part of the
wintering area in Africa. In order to separate these effects, two groups of
naïve storks were displaced to two different locations in Eurasia with no
breeding white stork population. These displaced birds were not delayed but
relied on their own orientation abilities without a chance of guiding by
experienced individuals.
We expected that the delayed storks should either first migrate towards the
SE and later change their flight direction towards the SSW (if they follow the
migratory program with delay) or migrate towards the SW from the very start
(if they just fly parallel to their free-living conspecifics). The displaced
birds were expected to fly parallel to the free-living white storks from the
Kaliningrad Region, at least until they encountered a major ecological barrier
(a large body of water or a mountain range). If the displaced juveniles are
able to navigate using an inherited ability to correct for displacements
(which we thought unlikely; Åkesson,
2003 and references therein), they should select the migratory
direction towards their first winter quarters in Sudan or Chad
(Berthold et al., 2001b
).
To test this hypothesis, it was necessary to trace the route of the
detained birds using satellite tracking (Berthold et al.,
1997,
2001a
,b
).
Satellite tracking has recently been applied to study the navigational
abilities of green sea turtles (Luschi et
al., 2001
; Åkesson et
al., 2003
; Hays et al.,
2003
) and petrels (Benhamou et
al., 2003
). This technology made it possible to track the animals
along the whole of their route and not to rely on recoveries. It appeared
possible to repeat the now classical studies of orientation and navigation in
migratory birds by displacement, recently reviewed by Åkesson
(2003
), on a new technical
level, as proposed recently (Mouritsen,
2001
,
2003
).
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Materials and methods |
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Two series of experiments (detention and displacement) were performed in
order to test whether inexperienced white storks follow an innate directional
program of migration. In 20002002, several groups of young birds were
taken from nests in the Kaliningrad Region of Russia [formerly East Prussia,
the same area where Thienemann
(1931) performed his
experiments]. They were raised in an aviary at the Biological Station Rybachy
(55°12' N, 20°46' E). The aviary was 23 mx4
mx4 m and housed a maximum of 18 storks simultaneously. Aviary height
allowed the birds to make short training flights. Food was provided four times
a day (when the birds were 56 weeks old) or three times a day (when
they were over 6 weeks old) and mainly included fresh fish. In all cases, the
amount of food given to storks was adjusted so that some pieces of fish were
left until the next feeding. They were removed before the next feeding, so
that only fresh food was available. Drinking water was available
constantly.
Delayed birds
Ten white stork nestlings were taken from their nests in the western part
of the Kaliningrad Region on 12 July 2000 at the age of 5 weeks. All
birds were taken from different nests. They were kept in the aviary until all
free-flying storks had left the Kaliningrad Region (which usually happens by
the end of August) and were released in three groups. Each group included two
individuals carrying satellite transmitters and one or two birds without
transmitters. All birds carried the usual aluminium rings for identification
purposes. The first group was released on 7 September, the second group on 14
September and the third group on 21 September, all at the same site in the
vicinity of Zelenogradsk, near the base of the Courish Spit (54°56'
N, 20°32' E).
On 10 July 2001, nestlings were taken from the same area of the Kaliningrad Region. Six birds were released in two groups on 3 September at two different sites in the western Kaliningrad Region. Each group included two birds with transmitters and one bird without a transmitter. All released storks carried aluminium rings. In 2002, nestlings were taken from nests on 1 July. Of the 10 birds, nine carried transmitters. They were released in four groups at different sites in the western Kaliningrad Region on 5 September.
Displaced birds
In 2001 and 2002, we carried out the displacement experiments. The aim was
to track the migratory route of inexperienced storks released at the normal
time (not delayed) but with no chance of being guided by conspecifics. It was
expected that the displaced birds, if capable, would follow their innate
migratory direction in spite of the displacement
(Perdeck, 1958).
In 2001, 10 first-year white storks were transported by air to Samara on 3
August and released in the Samara Region on 4 August 2001. This was done just
before the onset of the autumn migration of Kaliningrad storks. Five
individuals (four of them carrying transmitters) were released in Samarskaya
Luka National Park (Samara Region, 53°13' N, 49°53' E),
and the five other birds (four with transmitters) were released to the north
of Togliatti (Samara Region, 53°42' N, 49°15' E). Thus,
the white storks were displaced nearly 30° to the east. No breeding white
stork population exists in the Samara Region
(Borodin, 1994;
Lysenkov and Lapshin, 1997
).
Black storks (Ciconia nigra) breed in the Middle Volga region but
their numbers are extremely low. In most parts of the region they are probably
extinct (Lysenkov and Lapshin,
1997
). The experimental birds could have joined a group of black
storks and flown together with them, but this seems unlikely.
In 2002, white storks were transported by air to Omsk (southern part of Western Siberia) on 12 August. The birds were released in two groups in the Omsk Region. One group consisting of four storks (two with transmitters) was released on 4 August 2002 on the coast of Lake Tenis (56°12' N, 72°01' E), while the other group (two birds, one with transmitter) was released on 5 August near Ostrovnaya (56°23' N, 72°10' E). Omsk Region lies far to the east of the breeding range of white storks.
Details of the satellite tracking, transmitters used, ARGOS satellite-based
positioning system, etc. are described by Berthold et al.
(1997,
2001b
). We used PTT-100
transmitters produced by Microwave Telemetry Inc. (Columbia, OH, USA). Their
mass varied between 38 g (solar-powered transmitters) and 100 g
(battery-powered transmitters). As the mass of a white stork is usually
3.5 kg, transmitters weighed less than 3% of the birds' mass in all
cases.
Since the early 1990s, much work has been done on satellite tracking of
white storks (e.g. Berthold et al.,
2001b). Mortality during first-time autumn migration is
75%
in white storks (M. Kaatz, personal communication). We have no reason to
believe that mortality of storks equipped with transmitters is significantly
higher than in non-manipulated birds. Mortality of the displaced individuals
was high (nearly 100%). We cannot be sure but it seems that in many cases the
cause of mortality was hunting or collision with power lines. Signal usually
disappeared very abruptly, and it often happened when the birds reached more
populated areas, often with practically non-regulated hunting activities (e.g.
Batumi area in Georgia, Hassan-Kuli area in Turkmenistan, Karachi in
Pakistan).
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Results |
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Delayed birds
All storks released in September from the Kaliningrad Region in 2000 and
2001 moved towards the SW or WSW (Fig.
2). In 2000, the birds released on 7 September moved towards the
SW. The transmitter of one of the birds failed soon afterwards. The other
stork (# 14554) continued flying towards the SW. On 3 October it reached the
French Mediterranean coast south of Nîmes. On 7 October it took off from
the vicinity of St Tropez at 11:15 h and started its flight across the
Mediterranean. At 13:44 h on the following day the bird was already on the
African coast after flying a distance of 752 km. This bird spent its first
winter in Tunisia. Another bird released on 7 September without a transmitter
but with a metal ring (Moskwa B-60510) was found dead on 24 October 2001 in
south Baden (Baden-Württemberg, Germany).
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The two storks from the second group released on 14 September soon parted. Both birds took a WSW route. They moved only short distances and made long stopovers even when the weather allowed them to fly. One of the birds was found in an unhealthy condition in northern Poland on 12 October. Another bird reached Germany and was observed on 25 September near Wittenberg (Sachsen-Anhalt, Germany) and on 26 September near Taucha (Sachsen, Germany). It was finally found dead in Bavaria.
Birds from the third group, released on 21 September, moved towards the SW
only a very short distance, 100 km. Contact with them was lost at the
beginning of October when they were still in the Kaliningrad Region. The
transmitter from one of the birds was found by a member of the public
somewhere in the Kaliningrad Region and returned to the Biological Station
Rybachy two years later (the exact date and place of finding are not
known).
In 2001, six white storks were released in two groups (four of them with transmitters) on 3 September. Two tagged birds died before leaving the release site. Another two remained in the vicinity of the release site until 25 September. This may have been caused by very rainy weather, which is unfavourable for stork migration. On 25 September, the birds started to move towards the WSW. After reaching Germany, they remained there for more than 2 months without making significant movements.
Of the birds released in September 2000 and 2001 in the Kaliningrad Region, at least four individuals (or groups) chose the SW or WSW direction independently of each other. No other pattern was recorded. In 2002, the situation was different. Nine birds were released in four groups; seven of them were successfully tracked and at least six individuals/groups were flying independently of each other. Two birds initially chose a WSW direction but five flew more or less towards the south. Moreover, five birds out of seven changed their flight direction towards the SE when in Central Europe. This change was most dramatic in bird # 36169 (Fig. 3). Together with the wide scatter of initial directions, this makes the 2002 results quite different from those of the preceding years.
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Displaced birds
Of the storks released in the Samara Region in 2001, seven were tracked and
one transmitter failed two days after release
(Fig. 4). Five birds initially
chose the SSE direction, while two (flying together) chose the SSW direction.
One of the birds that initially departed towards the SSE, later changed
direction and flew to the SSW.
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At least until the birds reached the latitude of the Caspian Sea coast, their movements were influenced by topography. However, the initial flight directions could well have been the result of an innate program. It is noteworthy that the birds that moved to the SSE (the direction more or less corresponding to flight patterns of normally migrating Kaliningrad storks) left optimal habitats in the Volga valley and moved to dry steppe habitats probably not favourable for them.
Of the birds released in the forest steppe of Western Siberia, one died soon after release and two took a SSW route independently of each other (Fig. 4). Their flight pattern was clearly different from that expected on the basis of an innate program. One bird probably died in SW Iran, and the signal from the other was lost in Turkmenistan.
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Discussion |
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The results of our delaying experiments generally agree with those of Katz
(1986). However, the results
obtained by Thienemann (1931
)
and Schüz (1949
) were
different: only three SSWSW and no WSW recoveries were recorded (see
fig. 2B in Wallraff,
1977
).
Birds released on 14 and 21 September 2000, and those released on 3
September 2001 but delayed by inclement weather until 25 September, migrated
slowly and reluctantly. Delayed birds seem to be able to prolong their
migratory time program only within certain limits. Probably some of
Thienemann's and Katz's birds died in the vicinity of the release site but
were not detected. Katz (1986)
reported that five (out of 36) of his late-released storks were found dead
near his study area.
The directions taken by the displaced storks show the most variation. Flight paths shown by the birds released on the Volga could suggest that they followed an innate program guiding them towards the SSE (e.g. bird # 13105, Fig. 4).However, the birds released in Western Siberia flew as if they were navigating towards their African winter quarters (Fig. 4). From the viewpoint of the current theories (clock-and-compass vs innate navigation abilities), the results of these two similar experiments do not match.
We clearly need a theory capable of explaining the results of all the
experiments. It may be suggested, following Rüppell
(1937) and Rüppell and
Schüz (1948
), that
juvenile white storks have only a rough inherited migratory direction. None of
the experimental birds flew to the north, so the idea that they were
completely disoriented can be rejected with certainty. However, it seems that
they did not possess an exact migration map or program. This is suggested by
the large directional scatter shown by the delayed birds, even when their
treatment had been exactly the same (as, for example, in the 2002 experiment),
and by the widely varying behaviour shown by the displaced individuals. We
argue that this hypothesis can explain the results of numerous delaying
experiments (Thienemann, 1931
;
Schüz, 1949
,
1950
;
Wallraff, 1977
;
Katz, 1986
; our data) and our
displacement results.
Three possibilities may be imagined:
The hypothesis of Rüppell
(1937) that naïve
migrants have only a rough inherited migratory direction does not agree with
more recent findings in nocturnal passerine migrants
(Gwinner and Wiltschko, 1978
;
Helbig et al., 1994
). Much
evidence is available that many bird species have an inherited spatiotemporal
program that guides first-time migrants to their winter destination without
any aid from the adults (for reviews, see
Berthold, 1996
;
Mouritsen, 2003
). It may be
hypothesized that in soaring migrants that are heavily dependent on local
topography, social contacts and observation of the performance of migrating
conspecifics play a much greater role than in nocturnal migrants that usually
fly individually. This may presuppose a greater role for social inheritance in
the white stork and probably in other soaring migrants than in other
long-distance migrants.
Juvenile white storks normally migrate in large conspecific flocks containing experienced adult individuals. Therefore, naïve storks only rarely have to use their own innate orientation mechanisms. A result of this may be that selection pressure supposed to eliminate birds with failing orientation mechanisms may be rather weak as compared with the situation found in nocturnal passerine migrants. When we force juvenile white storks into using their innate orientation mechanisms, it may appear that comparatively many birds fail to orientate correctly.
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Acknowledgments |
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References |
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