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Significance of the White Sea as a stopover for Bewick's
Swans Cygnus columbianus bewickii in spring
BART A. NOLET'', VALERY A. ANDREEV2, PREBEN CLAUSEN3, MARTIN J. M. POOT4& ERIK G.J. WESSEL'
Netherlands lnstitute of Ecology, Centre for Limnology; Postbox 1299, NL-3600 BG Maarssen, The Netherlands
2Committee of Environment Protection and Natural Resources of Arkhangelsk Region,
Troitsky Avenue 49, Arkhangelsk, Russia
3National Environmental Research Institute, Department of Coastal Zone Ecology;
Grenivej 12, DK-8410 Ronde, Denmark
4Zoological Laboratory; University of Groningen, Postbox 14, NL-9750 AA Haren, The Netherlands
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We searched for a major stopover site of Bewicks Swans Cygnus columbianus bewickii in
the White Sea following the suggestion that one should exist on the stretch between
Estonia and the breeding grounds (1750 km). We discovered 733 Swans in Dvina Bay
during a late aerial survey in spring 1993. Subsequently, ground-based research was
carried out in May 1994, 1995 and 1996 in the Dry Sea, a tidal, shallow bay with fresh t o
brackish water just north of the Dvina Delta. The total number of passing Bewicks Swans
was estimated at 10974 (1994), 9593 (1995) and 17972 (1996) (32-60% of the flyway
population). Estimated peak numbers staging were 1500-2000 (9 May 1994), 4937 (1 7
May 1995) and 4457 (24 May 1996) (> 5-16% of the flyway population). The Swans
foraged almost exclusively on submerged water plants apart from some supplemental
feeding on emerged food plants around high tide. Stoneworts Chara spp. were an important
food in the late spring of 1996, because they grew in places where bog streams quickly
melted the ice. At this latitude (65"N) food alternatives to the submerged macrophytes
are rare in spring, but we cannot rule out the possibility that the Swans forage on grass
rhizomes on inundated pastures. One bird tracked by satellite staged 15 days in Dvina Bay,
of which four days were spent in the Dry Sea, in accordance with other indications that
the Dry Sea is part of a larger stopover site within Dvina Bay. Recent evidence shows that
the Swans largely slup the White Sea during autumn migration. However, in spring the
birds probably need this stopover to be able to carry reserves to the breeding grounds. At
present, the preservation of the submerged vegetation in Dvina Bay seems t o be crucial t o
the conservation of this Bewick's Swan population.
Tundra Swans Cygnus columbianus have a circumpolar
distribution. The nominate columbianus breeds on the
tundra of North America (> 150 000 birds). The swans
on the tundra of Europe and Asia belong to the subspecies bewickii; those breeding in the Lena Delta and
further to the east winter in Japan, Korea and China
(about 30000 birds), whereas the majority (also about
30 000 birds) of more westerly Bewick's Swans winter
in northwest Europe (Beekman 1997, Rees et al.
1997). A recent survey of important stopover sites of
waterfowl indicated no main site for Bewicks Swans
between Estonia and arctic Russia, a stretch of about
*Corresponding author.
Email: nolet@cl.nioo.knaw.nl
02001 British Ornithologists' Union
1750 km (Scott 81 Rose 1996). In theory, Bewicks
Swans should be able to cover this distance in one nonstop flight but, based on the timing of the migration,
Beekman et al. (1991) suggested that a further major
stopover site should exist. Rees (1991) reported that
nine marked Bewick's Swans had been observed
between Estonia and the breeding grounds, but a major
stopover site was not identified. Beekman et al. (1991)
thought that a stopover was located somewhere in
Karelia and/or in the White Sea, based on the
presumed preference of migrating Bewick's Swan for
tubers of Fennel Pondweed Potamogeton pectinatus and
the conceivable lack of alternative food sources
(terrestrial or agricultural plants) above 60"N in the
migratory period (see also Beekman et al. 1996).
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B.A. Nolet et al
In our search for the missing link, we first performed
an aerial survey of the White Sea in spring 1993. We
subsequently visited the most promising site in the
springs of 1994, 1995 and 1996. Our aim was twofold.
First, we wanted to assess the numerical importance of
this spring stopover site for Bewick's Swans. Secondly,
we studied the food choice in relation to ice break-up
in order to obtain data on food preference and the
Swans' dependence on submerged water plants.
STUDY AREA
In the White Sea, submerged vegetation is present in
Ukhta and Unskaya Bay on the Onega peninsula
(Zostera spp.; Beekman et ul. 1996) as well as in the
southwestern part of Dvina Bay (Fig. 1). Here waterplants are found in the delta o f the Severnaya
(Northern) Dvina river and in the nearby Dry Sea east
of the island Mud'yug. The latter was our main study
area.
The Dry Sea (64"51'N, 40"17'E) is a tidal area with
an amplitude varying between 0.3 and 1.2 m. We
divided the area into south, central and northern parts
(Fig. 1, inset). There are clear vegetation zones with
(from high to low) Reed Phrugmites australis, Bulrush
Scirpus lacustris or stoneworts Chara spp., Fennel
Pondweed Potumogeton pectinatus and, in the brackish
waters, Eelgrass Zosteru marina. O n at least one site,
Fennel Pondweed is replaced by the hybrid of Fennel
Pondweed and Fineleaf Pondweed Potumogeton
filiformis, i.e. Potamogeton x suecicus. As a result of the
discharge of the Northern Dvina and numerous small
streams in spring after ice break-up, the water in the
Dry Sea is practically fresh (0-8 mM salt) a t that time
of the year, except at the entrance and in the middle of
the bay in the north part where the water was braclush
(50-60 mM salt). Salt concentrations were calculated
from the measured conductivity and water temperature on 3 June 1996 using linear regression equations
derived from Tables 3.1 and 3.2 in Golterman (1970)
METHODS
Aerial surveys
The aerial surveys were conducted on 3 1 May, 1 and 2
June 1993, and 7 June 1996 with AN2 and L410
planes, respectively In 1993, the whole coastline of the
southeastern part of the White Sea from Kem to and
including MeLen Bay was covered, whereas in 1996
only the stretch between Dvina Bay and Mezen Bay
was counted (Fig. 1) Flight altitude was 50-1 00 m and
@ 2001 British Ornithologists'
flight speed about 80 km/h. The trajectory was
200-500 m away from the coast, but in 1996 an inland
route was taken over the tundra between Dvina Bay
and Mezen Bay (Fig. 1). A pair of observers was situated
on each side o f the plane. The number of birds counted,
and the time of observation, were noted. The observations were checked for double counts and mapped.
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Fieldwork
We counted the number of passing swans from a 10 m
high tower on the weather station at the southern tip
of the island Mud'yug using 7-10x binoculars and
2 0 - 6 0 ~telescopes. Bewick's Swans were distinguished
from Whooper Swans Cygnus cygnus (less than I Yo of
the swans). Counts were conducted every day between
05:OO and 22:OO h from 7 May to 5 June 1994 (393 h),
4-17 May 1995 (125 h) and 1-27 May 1996 (260 h).
We assumed that no swans migrated over sea during
the dark night hours (see Pennycuick et al. 1999). In
1994 continuous counts were made during the day,
whereas in 1995 and 1996 two hours of observation
were followed by a one-hour pause and we used a
linear interpolation to estimate the numbers passing
during these observation gaps.
The swans were foraging in flocks around low tide.
These were counted occasionally in 1994 and almost
daily in 1995 and 1996. Flocks were mapped by taking
two bearings from the shore, using landmarks as reference points, or by measuring the angle (corrected for
the local declination of +14") to this flock from observation posts using a range finder (Leica Geovid 7 x 42
BDA). The map location of these observation posts
was in turn determined using a Garmin GPS 40.
At the end of May and the beginning of June xve
mapped the submerged vegetation along transects,
using the rangefinder or a compass and a 100-m long
rope for navigation. The borders of the beds in the
north part of the Dry Sea were also surveyed from a
small boat during high tide, again using compass
bearings. The species composition and remaining plant
biomass were determined by taking samples at regular
intervals (10-100 m, depending on the size o f the
bed). In Eelgrass beds, we placed a square steel frame
(0.1 m2) a t the bottom (total sampled area: 8.0 m' in
1995 and 4.4 m? in 1996). After taking care that
ramets growing inside or outside the frame ended up a t
the appropriate site of the frame during placement, Lve
cut a square of turf along the inside of the frame.
In stonewort and pondweed beds we took sediment
cores 25-40 cm deep and 10-14 cm in diameter (total
sampled area: 3.5 mx in 1995 and 3.2 m* in 1996). The
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Union, Ibis, 143, 63-71
Staging areas for swans in the White Sea
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Figure 1. The White Sea with the trajectories of the aerial surveys conducted between 31 May and 2 June 1993 (- - -) and on 7 June
1996 (. . .). Inset shows the Dry Sea (Guba Sukhoye More). Light grey indicates shallows that fall dry during extreme low tides. The
locations of the major swan feeding sites are indicated (P, Fennel Pondweed Potamogeton pectinatus except P8 where it is
Potamogeton x suecicus; C, stoneworts Chara spp.; Z, Eelgrass Zostera marina). m, Location of the observation post on the weather
station.
cores were then sieved through a .I-mm sieve (in the
north part of the Dry Sea) or a 3-mm sieve (in the
south and central part of the Dry Sea). Samples
(subsamples for pondweed tubers) were dried to
constant weight a t 70°C and biomass density given
as dry weight. Pondweed tuber densities were logtransformed (to achieve normality; thus, zero values
were excluded) and differences between years (1995
and 1996) and beds (P4, P5 and P6) were tested with
an analysis of variance after checlung for normality
(Kolmogorov-Smirnov test) and homogeneity of variances (Levene's test).
We recorded the behaviour of the swans by scan
sampling (Altmann 1974), distinguishing foraging (i.e.
paddling, head-dipping or up-ending, see Rees et al.
1997) from non-foraging behaviour. Scans were made
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B.A. Nolet et al.
a t the pondweed beds P4, P5 and P6 and the Eelgrass
bed Z1 (Fig. 1, inset) between 18 and 24 May 1995.
We made additional scans a t the pondweed beds
between 17 and 28 May 1996. The distance from the
observer to the swans was 250-1500 m at the
pondweed beds and 3000 m a t the Eelgrass bed. Swans
were scanned once every 15 or 30 minutes using a
2 0 - 6 0 ~ telescope. When more than 100 swans were
present, we usually first counted the swans and subsequently scanned 100 of them evenly distributed over
the flocks. We calculated the average for each quarter
of an hour, weighting the scans according to the number
of swans present (pondweed: 167 scans in total with
on average 165 swans, range 7-718; Eelgrass: 86 scans
in total with on average 214 swans, range 100-600).
Table 1. Ice break-up in the three years of study
1994
~
~~
~~~~~
Ice break-up at Northern
Dvina river
First openings in Dry Sea
Dry Sea largely ice-free
-~
1995
~~
~
1996
~
c 1 May
23 April
8 May
9 Maya
11 May
c 1 May
c 4 May
9 May
24 May
aOpenings may have been earlier in the north part.
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Chemical analysis
Eelgrass leaves collected in 1995 and 1996 were dried
and later analysed for Kjeldahl nitrogen, cell wall components (neutral detergent fibre NDF, acid detergent
fibre ADF and lignin; Van Soest &Wine 1967), and fat
(ether extraction) and ash content. Protein content was
calculated as 6.25 x Kjeldahl nitrogen, hemicellulose
content as the difference between NDF and ADF,
cellulose content as the difference between ADF and
lignin, and soluble carbohydrate content as the part
remaining after subtraction of protein, fat and NDF
content. Pondweed tubers collected from different
beds in 1995 were analysed only for ash and ADF
content.
RESULTS
that the ice disappeared first in the south part and last
in the north part. However, small openings in the ice
formed as early as 9 May 1996 above the stonewort
bed C1 in the north part where small bog streams
entered the Dry Sea. The first openings above
pondweed beds developed on 14 May in the south
(Pl) and central part (P3). The small Eelgrass bed 2 2
in the central part was ice-free as early as 15 May, but
no part of the large Eelgrass bed Z1 in the north part
was exposed until 18 May. Finally, the pondweed bed
P9 and the adjacent stonewort bed C4 in the north
part became only ice-free on 20 May.
Swan passage
In May 1994, 10 974 Bewick’s Swans were counted
flying in a northerly or easterly direction along the
island of Mud’yug; 786 individuals flew in the opposite
direction. In May 1995 and 1996, respectively, we
counted 6944 and 14 1 12 Bewick’s Swans landing or
flying into and 156 and 1071 flying out of the Dry Sea.
Correcting for the observation gaps, we estimated the
total number of northerly or easterly flying Bewick’s
Swans at 10974 in 1994, 9593 in 1995 and 17972 in
1996. This represents 37%, 320/0 and 60Y0, respectively,
of the flyway population, estimated at 30 000 birds.
For 1994 and 1995 these are minimum estimates, since
migration had already started when the counts started
in 1994 and continued after we stopped counting in
1995.
In 1994, peak migration occurred on 10 May. The
majority of swans passing the observation post at the
weather station between 7 and 9 May flew over
the largely ice-covered Dry Sea and continued their
journey northeastwards. Despite the large difference in
the onset of spring in 1995 and 1996, the majority of
Bewick’s Swans passed through in the second decade
of May of 1995 and 1996 with peak numbers on 17
and 18 May, respectively. Most of the swans passing on
14 May 1996 entered an ice-covered Dry Sea, and flew
on into the northeast.
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Aerial surveys
In 1993, concentrations of Bewick’s Swans were only
seen in Dvina Bay on 1 June: 118 in the Dvina Delta
and 61 5 (including one bird with a blue neck-collar) in
the Dry Sea (Fig. 2). The birds were partly resting
along the water edge, partly floating on the water. In
1996, the aerial survey was conducted after the swans
had left the Dry Sea. O n 7 June, we counted only very
small numbers of Bewick’s Swans north of the Dry Sea:
76 on small tundra lakes between Dvina Bay and
Mezen Bay, and another 23 along the east coast of
Mezen Bay.
Ice break-up
Spring was relatively early in 1995, late in 1996 and
intermediate in 1994 (Table 1). In 1996, we observed
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@ 2001 British Ornithologists’ Union, Ibis. 143, 63-71
Staging areas for swans in the White Sea
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Figure 2. Black ellipses depict the concentrations of Bewick’s Swans in Dvina Bay during the aerial survey of 1 June 1993:flock sizes
are: (1) 118,(2) 295 and (3)320 swans. Letters indicate the locations of Bewicks Swan 1 1 OU tracked by the ARGOS satellite system
during its stopover of two-weeks in Dvina Bay in spring 1996.Subsequent locations are labelled in alphabetical order. Accuracy of location represented as black (150-350 m), grey (35&1000m) or white (> l km). Star indicates position determined by visual observation
4.5 h before satellite location v.
Swan staging and foraging
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In 1994, between 1500 and 2000 Bewick’s Swans were
staging in a large opening in the ice in the Dry Sea on
9 May. Up to 15 May, about 900 Bewick’s Swans were
present, mainly feeding on pondweed tubers.
In 1995, the maximum number of staging Bewick’s
Swans in the south and central part of the Dry Sea was
counted on 15 May with 3865 birds foraging on
pondweed (Fig. 3). Unfortunately, the north-part of
the Dry Sea was not counted until 18 May, when we
observed 1325 Bewick’s Swans feeding on Eelgrass
there (Fig. 3). Under the assumption that this number
was the maximum number of Bewicks Swans in the
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B.A. Noletet al
north part in 1995, we estimated by linear interpolation that the maximum total number of staging
Bewick's Swans in the Dry Sea in 1995 was 4937 on 17
May. In 1995, the estimated total number of swan-days
in the Dry Sea was 52 089, of which a t least 9.9% were
spent on Eelgrass.
In 1996, the number of staging Bewick's Swans in
the south and central part was less than half the
number in the previous year. A maximum of 1610
birds was counted on 19 May. Again, these swans were
mainly feeding on pondweed tubers (Fig. 3). However,
on 16 May, during the early stages of ice break-up,
most swans were foraging on the small Eelgrass bed
( Z 2 ) . Many movements were observed between birds
feeding on ZZ and birds exploring the pondweed beds
P4, P5 and P6, which had become available again in
the course of the day after ice, formed during the
night, had melted away. In contrast, the numbers in the
north part were much greater in 1996 than in 1995
with 3600 swans staging on 24 May. Here they started
feeding on stonewort bulbils, which became available
first. The swans switched to the pondweed bed P9 as
soon as it was exposed on 20 May, but it was difficult
to judge which proportion of the flock was feeding on
the adjacent stonewort bed C4. The maximum
number in the Dry Sea as a whole (4457 staging birds)
was reached on 24 May, i.e. one week later than in
1995. The total number of swan-days was 32 910 in
1996, 8.8%of which were spent on Eelgrass.
The submerged water plants were only available to
the Bewick's Swans at low tide, and their behaviour
was strongly related to the tidal cycle. In both 1995
and 1996, the swans in the central part were feeding
on rhizomes of Reed and (later in the 1995 season)
emerging leaves of Bulrush around high tide (Fig. 4).
During one cycle, a swan actively foraged for, on average, 4.0 h on Fennel Pondweed and another 0.6 h on
Reed and Bulrush; with a tidal cycle of 12 h 15 min,
this corresponds to 7.9 h and 1.2 h per day, respectively. Eelgrass was available for longer periods than
Fennel Pondweed (Fig. 4), namely 6.5 h/cycle, equivalent to 12.8 h/day. Our preliminary chemical analyses
suggest that Eelgrass leaves had a relatively low soluble
carbohydrate content, b u t high protein content
compared with pondweed tubers (Table 2).
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0on ice
2000-7 north
$
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i
mL
+
0
&
a
$
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Significance of Dvina Bay as a spring stopover
site
Our migratory counts indicate that between 32% and
aReed
=
stoneworts
Eelgrass
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4000,
north
2000
1 south
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a 4000- central
3
(I)
pondweed
DISCUSSION
3000-
2000-
1000-
II
0
2000
1 south
1000 -
7
1000 -
?
0
5
10
15
20
May 1995
25
30
35
0
5
10
15
20
25
30
35
May 1996
Figure 3. Number and diet of Bewick's Swans staging in the three parts of the Dry Sea in May 1995 and 1996. The swans feeding on
pondweed in the north part were partly foraging on an adjacent stonewort bed. The birds counted on 8 May 1995 in the north part were
roosting during high tide.
@ 2001 British Ornithologists' Union. /b/s. 143, 63-71
Staging areas for swans in the White Sea
0Reed/Bulrush
pondweed
-6
-4
0
2
-4
-2
0
2
1994 and 1996 showed that peak numbers of staging
Bewicks Swans in the Dry Sea were reached more
than two weeks later than in Estonia. In 1994, numbers
peaked sharply in Estonia and in the Dry Sea on 24
April (Luigujije et al. 1996) and 9 May, respectively. In
1996, numbers remained high in Estonia between 27
April and 7 May', and peaked in the Dry Sea on 24
May. The swans might have spent the intervening time
in the Gulf of Finland (Rees 1991), but there are indications that a large part stages elsewhere in Dvina Bay.
The most direct evidence comes from a swan (1 lOU)
tracked by satellite in spring 1996. Beekman and
Laubek (1997) report that it flew from Estonia to Dvina
Bay in only three days. A detailed analysis revealed that
this swan used exactly the same areas that swans had
been observed in during the aerial survey three years
earlier. It spent three days in the south part of the Dry
Sea, subsequently staged in the Dvina Delta for 11
days and then moved to the north part of the Dry Sea
for a short stop prior to its flight to the Pechora Bay
(Fig. 2).
Of its two-week staging period in Dvina Bay, this
satellite bird thus spent only a few days in the Dry Sea,
and this seems to be true for the majority of the swans.
Division of the total number of swan-days by the
number of passing swans yields an average staging
period of five days in 1995 and two days in 1996. Since
we observed that some of the swans did not land in the
Dry Sea, or only landed briefly in order to drink, the
staging period of individual swans that did forage must
have been longer. However, observations of neckcollared birds confirm the short staging period in the
Dry Sea (Nolet & Drent 1998).
The peak numbers of Bewick's Swans present in the
Dry Sea are close to 5000 birds. This justifies a classification as a major stopover site sensu Scott and Rose
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"
-6
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0other
-2
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4
6
Time to low tide (h)
Figure 4. The behaviour of Bewicks Swans in relation to the
tide. (a) Scans in the central part of the Dry Sea in May 1995
and 1996 (1-1 1 scans per bar; the black bar indicates no observation). Non-foraging behaviour is split into resting and other
behaviour. (b) Scans in the north part in May 1995 (1-6 scans
per bar).
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60% of the West-European flyway population of
Bewick's Swans passes through Dvina Bay in May.
Simultaneous counts a t Mud'yug and in Estonia in
Table 2. Chemical composition of main food items of Bewick's Swans.
Chemical composition (% organic dry matter)
-
Protein
Fat
Soluble carbohydrates
NDF
ADF
Lignin
Hemicellulose
Cellulose
Eelgrass leaves
( n = 2)
Pondweed tubers
(Van Eerden et a/. 1997)
28.6 3.4
2.1 1.1
26.3 i 2.7
43.0 * 1.8
31.9* 1.6
3.6 1.9
11.1 i 3.4
28.3 * 0.4
14.8
5.0a
36.9
43.2
6.7b
*
*
-
36.5
aAssumed.
bWe measured 6.1 & 1.8 in pondweed tubers ( n = 6) collected in the Dry Sea.
@ 2001 British Ornithologists' Union, Ibis, 143, 63-71
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6.A. Nolet et al
( I 996) (> 10 %I of the flyway population). However, as
discussed above, the Dry Sea is probably only part of a
spring stopover. Peak numbers around and within
Dvina Bay as a whole are likely to be closer to 10 000
birds. The utilization of the bays on the Onega peninsula and Dvina Delta by Bewick’s Swans urgently
needs confirmation by aerial counts that are conducted
earlier and more frequently in the migratory season
than our own survey.
during autumn stopover in the Veluwemeer, The
Netherlands (Van der Winden et al. 1997). Unfortunately, data on the nutritional value of stonewort
bulbils are lacking. Secondly, at a time when the wintering population of swans was much smaller than it is
now, and prior to the decline of aquatic vegetation in
western Europe, Bewick’s Swans were also foraging on
both pondweed and Eelgrass (Brouwer & Tinbergen
1939, Sparck 1958).
Whether Bewicks Swans prefer pondweed over
Eelgrass remains uncertain. We found that the swans
can exploit Eelgrass considerably longer (12.8 h/day)
than pondweed tubers (7.9 h/day plus 1.2 h/day on
Reed rhizomes and Bulrush leaves). The swans can
extend the foraging period on Eelgrass by eating the
leaves during rising and falling tides. This advantage
may at least partly offset any disadvantage due to a
lower soluble carbohydrate content of Eelgrass leaves.
The leaves, which start growing while under the ice
(McRoy 1969), may also be attractive because they
contain about twice as much protein as pondweed
tubers. In absolute numbers, swan usage of Eelgrass
was most pronounced in 1995. In that year Eelgrass
was more abundant than in 1996 (1 9.5 g/m* + 22.1 sd
versus 10.9 17.3, PZ = 44 in both years, t,,- = 2.02,
P < O.O5), even after exploitation by swans, maybe
because of less ice-scouring damage and an earlier
onset of the growth of Eelgrass in the early spring of
1995. The average pondweed tuber densities varied
between 5.5 and 20.1 g/mz. The three pondweed beds
that were sampled in both 1995 and 1996 after the
swans had left, did not differ in tuber density between
years (F,,,?, = 1.49, ns; corrected for differences
between beds), despite the large difference in swan
exploitation (22 958 versus 6123 swan-days on
pondweed tubers in the central part in 1995 and 1996,
respectively). This indicates that, during the staging
period, more pondweed tubers must also have been
present in 1995 than in 1996.
If the swans depleted the pondweed tubers during an
autumn stopover in the Dry Sea, no tubers would have
been available during the spring since the tuber stock
would not grow in the meantime but would decrease
due to winter mortality and respiration of the tubers
(Beekman et al. 1991). Local fishermen told us that
the number of swans in the Dry Sea is much smaller in
autumn than in spring. Recent results with satellite
tracking show that, during the autumn migration,
Bewick’s Swans skip the White Sea or only stop there
for two days’. The use of Dvina Bay as a stopover in
spring only can be esplained by the advantage
conferred on the swans of carrying body reserves to the
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Diet
The Bewick’s Swans staging in the Dry Sea foraged
almost exclusively on submerged water plants. These
become available to the swans as soon as the ice breaks.
We recorded only supplemental feeding on emerged
food plants (rhizomes of Reed and, in the early spring
of 1995, sprouting leaves of Bulrush) around high tide.
During their stopover in Estonia, the swans also mainly
refuel on submerged vegetation (pondweed and
stoneworts), but additional feeding on cultivated
plants has occurred since 1978 (Rootsmae 1990 in
Luigujoe et al. 1996). The preponderance of agricultural plants in the diet of the swans fluctuates from
year to year, both in autumn and spring, strongly
depending on the weather (Luiguj6e et al. 1996). In
our case, swans were never seen foraging on terrestrial
food plants. Agriculture around Arkhangel’sk is limited mainly to the pastures along the Northern Dvina
and in its delta. These pastures might be used by swans
when flooded in spring, since grass rhizomes have been
found to be important spring food for swans a t lower
latitudes (Rees et al. 1997). However, the data at hand
point to an increase in the importance of submerged
vegetation as food for refuelling swans with latitude
(cf. Beekman et al. 1996).
The opportunistic food choice among submerged
plants we observed may be due to the strong increase
of the population in the last decade (Beekman 19973,
some birds being forced to feed on less preferred water
plants than Fennel Pondweed. We think that this is
only part of the explanation for the two following
reasons. First, the swans exploited the stoneworts only
in the late spring of 1996 when they had no good food
alternatives due to ice-cover. The swans apparently
included pondweed tubers in their diet as soon as the
nearby pondweed bed became ice-free, although not
all stonewort beds had been depleted, as indicated by
the high biomass remaining at C1 (40.6 g/m’ 69.7 sd,
n = 24) compared with C3 (3.2 f 4.9, n = 16) and C4
(4.0 3.6, n = 16). Bewick’s Swans also showed a preference for pondweed tubers over stonewort bulbils
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02001 British Ornithologists’ Unlon, ibis,
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143, 63-71
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Staging areas for swans in the White Sea
breeding grounds (Cooke et al. 1995). Arrival on the
breeding grounds is about ten days after the peak in
staging numbers in the D r y Sea (cf. Rees et al. 1997).
We conclude t h a t Dvina Bay contains a major spring
stopover site for Bewicks Swans. W h i c h other shallows
in Dvina Bay besides the D r y Sea are important, and to
w h a t extent flooded pastures along the Northern
Dvina river are utilized b y swans, remains to be investigated further. At the moment, however, the
preservation of the submerged vegetation in Dvina Bay
seems to be crucial to the conservation of this Bewicks
Swan population.
We greatly acknowledge the Meteorological Office, and in
particular Pjotr A. and Marij D. Malygin of the Mud'yug
weather station for their hospitality. We also thank Sergej V.
Dokunihin and Yurij V. Asutchenko for their valuable logistic support. We thank Ebbe Bagebjerg, Alexander S.
Cherenkov, Anne Dekinga, Rudi Drent, Piet Duiven, Martin
Epe, Frederik Haas, Anita Koolhaas, Harry Korthals, Oscar
Langevoord, Roef Mulder, Jeroen Nienhuis, Vladimir A.
Semashko and Eugeny E. Syroechkovslu Jr for their good
company and hard work in the field. Jan Beekman kindly
placed his spring satellite trackmg data at our disposal, and
Leho Luiguj6e gave us access to his report on the counts of
swans in Estonia in 1996. Peter Mikkelsen digitized the maps.
Jan Beekman, Kees Carnphuysen, Marcel Klaassen and Eileen
Rees commented on drafts of &s paper. The study was funded
by the Netherlands Organization for Scientific Research
(NWO grant 047-002-008 to B.A.N.), the Danish Natural
Science Research Council (grant 950342 1 to P.C.), the
Beijerink Popping Fonds and the Swedish Natural Science
Research Council (grant to h e Lindstrom, Lund University).
This is publication number 2610 of the Netherlands Institute
of Ecology.
71
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zyxwvutsrq
ENDNOTES
1L. Luiguj6e & A. Kuresoo, unpublished report, Institute of
Zoology and Botany, Estonian Academy of Sciences, Tartu.
2B.A. Nolet, J.H. Beekman, M. Klaassen, B. Laubek, 0.
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Netherlands Institute of Ecology.
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Received 7 June 1999; revision accepted 17 January 2000
@ 2001 British Ornithologists' Union, Ibis, 143, 63-71